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IMPACT OF ALIEN SLUGS ON NATIVE PLANT SEEDLINGS IN A DIVERSE
MESIC FOREST, O‘AHU, HAWAI‘I, AND A STUDY OF SLUG FOOD PLANT
PREFERENCES
A THESIS SUBITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY
OF HAWAI‘I IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE
DEGREE OF
MASTER OF SCIENCE
IN
BOTANICAL SCIENCES
(BOTANY-ECOLOGY, EVOLUTION, AND CONSERVATION BIOLOGY)
MAY 2006
By
Stephanie M. Joe
Thesis Committee:
Curtis C. Daehler, Chairperson
Donald R. Drake
David C. Duffy
Robert H. Cowie
We certify that we have read this thesis and that , in our opinion, it is satisfactory
in scope and quality as a thesis for degree of Master of Science in Botanical
Sciences (Botany-Ecology, Evolution, and Conservation Biology)
THESIS COMMITTEE
Chairperson
ACKNOWLEDGEMENTS
Funding for this study was received from the Ecology, Evolution and
Conservation Biology Research Grant, the Beatrice Krauss Fellowship in Botany
and the Sigma Xi Grants in Aid of Research. My committee has been absolutely
vital throughout. I am grateful to my advisor Curtis C. Daehler for his enthusiasm
and diligence, Robert H. Cowie for sound advice and thorough editing, Donald R.
Drake for encouraging me to study slugs rather than worms and David C. Duffy
for sticking by me through the whole ordeal. Additionally, I thank the U.S. Army
Garrison Natural Resource Staff, without whom this project would never have
succeeded. They grew the plants, provided materials and staff and helped collect
data. In particular, I am grateful to Naomi Arcand, Seth Cato, Vincent Costello,
Hoala Fraiola, Victor Göbel, Julia Gustine, Kapua Kawelo, Matthew Keir, David
K. Palumbo, Leanne Obra, Jobriath Rohrer, Dominic Souza, Robert Romualdo,
William Weaver and Lauren Weisenberger for their help. Students, researchers
and staff from the University of Hawai‘i helped out as well. I would like to thank
Kyle K. Koza, Victor Cizankas, Will Haines, Mitsuko Yorkston, Charles Chimera
and Karen Brimacombe. Above all, I thank my husband, Paul D. Krushelnycky.
iii
ABSTRACT
Introduced species have the potential to cause serious ecological disruption,
particularly on oceanic islands. When introduced species invade natural areas,
endemic species may be threatened, especially when the invasive species
represent guilds or functional groups that were previously lacking. Hawai‘i has no
native slugs, but over a dozen species are now established. Slugs are important
seedling predators in their native habitats, and in introduced habitats they can
cause major shifts in the abundance some plant species. In order to better
investigate slug impacts on native plants in Hawai‘i, I carried out research which
1. identified differences in the acceptability of five native plant species to five
alien slug species 2. assessed the effect of slug herbivory on the growth and
survival of three native and two alien plant species, and 3. measured changes in
seedling regeneration due to slug herbivory.
Results from feeding assays indicated a significant difference in palatability
among plant species, but no statistical difference in overall feeding preference
among slug species. Urera kaalae (Urticaceae) was found to be significantly
more palatable than the other four plant species and, thus, is predicted to be
more vulnerable to slug herbivory in the field.
I tracked the fate of planted seedlings and natural germinants from the seed bank
in both slug-excluded and slug-accessible plots in diverse mesic forest in the
iv
Wai‘anae Mountains on the island of O‘ahu. Among seedlings that survived to
the end of the experiment, there was no significant difference between slugherbivory treatments in growth index measurements. There was little germination
from the seed bank, with no statistical difference in total number of seedlings
between treatments. However, two of the three native species, Schidea obovata
(Caryophyllaceae) and Cyanea superba (Campanulaceae) had significant
reductions in survival of 49% and 53%, respectively, in the slug-exposed
treatment. Survival of two invasive species, Clidemia hirta (Meslastomataceae)
and Psidium cattleianum (Myrtaceae) was not significantly affected by slugs. This
study demonstrates that slugs may pose a serious threat to native plant species
by reducing their survival and thereby facilitate the success of certain invasive
species.
v
TABLE OF CONTENTS
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
iii
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
iv
List of Tables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
viii
List of Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
viii
Chapter 1: Literature review and discussion of hypotheses . . . . . . . . . . . . .
1
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1
Study organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2
Impacts of slug herbivory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3
Slugs in Hawai‘i . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5
Hypotheses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7
Chapter 2: Palatability of native plant species to alien slug species . . . . . . .
16
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
16
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
18
Study organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
18
Feeding trial protocol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
21
Statistical Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
24
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
24
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Chapter 3: Impact of alien slugs on native plant seedlings . . . . . . . . . . . . . .
37
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
37
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
40
Field site . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
Study species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
Seedling preparation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
43
Experimental design . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
44
Slug monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
47
Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
47
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
49
Plant growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
49
Herbivory damage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
49
vi
Seedling survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
50
Seed bank regeneration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
Slug monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
51
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
Appendix A: Change in plant size index over time . . . . . . . . . . . . . .
63
Appendix B: Change in leaf number over time . . . . . . . . . . . . . . . . .
68
Appendix C: Change in herbivore damage over time . . . . . . . . . . . .
73
Literature cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
78
vii
LIST OF TABLES
Table
Page
1.1
Gastropod families containing slugs . . . . . . . . . . . . . . . . . . . . . . .
9
1.2
List of slugs found within the state of Hawai‘i . . . . . . . . . . . . . . . . . 10
1.3
List of native species threatened by alien slugs . . . . . . . . . . . . . . . 11
2.1
Mean acceptability indices (AI) for 25 slug-plant species pairs . . .
30
2.2
ANOVA using AI scores from 25 slug-plant species pairs . . . . . . .
31
2.3
Secondary plant compounds repellent to slugs . . . . . . . . . . . . . . .
31
3.1
Seedling height (mm) by species on day 0 of the study . . . . . . . . . 55
3.2
Two-way ANOVA of seedling survival by herbivory treatment . . . . 55
3.3
Number of germinants from seed bank by herbivory treatment . . .
55
LIST OF FIGURES
Page
Figure
2.1
Slug collection sites on the Island of O‘ahu . . . . . . . . . . . . . . . . .
2.2
Percent of slugs engaged in feeding . . . . . . . . . . . . . . . . . . . . . . . 33
2.3
Mean AI scores for each plant species (all slug species) . . . . . . .
34
2.4
Distribution of AI scores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
35
2.5
Boxplot showing weight distribution of slug species . . . . . . . . . . .
36
3.1
Location of Kahanahāiki Management Unit . . . . . . . . . . . . . . . . .
56
3.2
Plant growth in slug-exposed vs. slug-excluded plots . . . . . . . . . . 57
3.3
Leaf change in slug-exposed vs. slug-excluded plots . . . . . . . . . . 58
3.4
Herbivory damage in slug-exposed vs. slug-excluded plots . . . . .
59
3.5
Survival in slug-exposed vs. slug-excluded plots . . . . . . . . . . . . .
60
3.6
Survival over time by plant species . . . . . . . . . . . . . . . . . . . . . . . . 61
3.7
Slug counts at refugia over time . . . . . . . . . . . . . . . . . . . . . . . . .
viii
32
62
CHAPTER 1
LITERATURE REVIEW AND DISCUSSION OF HYPOTHESES
INTRODUCTION
The deliberate and accidental introduction of alien species into new habitats
where they establish and spread is a significant component of human-caused
global change (Vitousek et al. 1997). Through predation on and competition with
native species, introduced species accelerate extinction rates and reduce global
biodiversity (Gurevitch and Padilla 2004). For instance, approximately 42% of the
species on the U.S. Threatened and Endangered species lists are at risk
primarily because of the activities of introduced species (Pimentel et al. 2004). In
other regions of the world, introduced species seriously threaten up to 80% of
native endangered species (Armstrong 1995).
The endangerment and loss of native species is particularly acute on oceanic
islands, which have unusually high rates of endemism (Kaneshiro 1988). In the
Hawaiian Islands, where a considerable portion of intact native ecosystems are
under State and Federal protection (Cuddihy and Stone 1990), invasive species
are now the primary threat to the persistence of the native flora and fauna (Loope
1992). For native Hawaiian plants, competition from invasive plants and
herbivory by invasive animals are two of the most important forces responsible
for declining populations (Bruegmann et al. 2002).
1
Herbivory is central to the organization of biotic communities (Marquis 1992;
Janzen 1970). By influencing plant species composition, it also has indirect
effects on most other species in a community. While vertebrate herbivores are
frequently the focus of studies regarding plant community dynamics (Kotanen
1995; Stone 1985), the impacts of invertebrates are important as well. Among
invertebrate herbivores, terrestrial molluscs, such as slugs and snails, are some
of the most important grazers of temperate grassland species (del-Val and
Crawley 2004; Hitchmough 2003). Because these animals are known to target
seedlings (Hanley et al. 1995), they can have profound consequences for native
plant recruitment and therefore adult species composition (Hanley et al. 2002;
Hanley et al. 1996). They may also play an important role in the success or
failure of rare plant restoration efforts.
Study organisms
Slugs are a polyphyletic group of terrestrial gastropods descended from snails.
The absence of a shell gives them their distinctive form, which arose by way of
convergent evolution in multiple snail lineages (Runham and Hunter 1970). As a
result of this evolutionary history, there exists a continuum of gastropod forms in
terms of shell reduction, with snails at one end, slugs at the other, and various
intermediate forms, sometimes referred to as “semi-slugs”, in between. Thus, the
number of gastropod species considered to be slugs is not definitive. To avoid
confusion, my use of the term is limited to those families considered to be slugs
by South (1992) (Table 1.1).
2
The repeated evolution of the slug form in several gastropod lineages is a
testament to its utility, particularly in calcium-poor, wet environments, such as
those found on many volcanic islands. Both slugs and snails are hermaphroditic
and many species can self-fertilize (Jordaens et al. 2000) as well as tolerate a
wide range of temperatures (Rollo and Shibata 1990). These traits make slugs
excellent colonizers and potential invaders when introduced into new areas.
Slugs will feed on a variety of foods including carrion, animal feces, lichens, a
variety of small animals and other slugs (South 1992). With the exception of a
few geographically restricted groups, however, most slugs are considered to be
generalist herbivores (Rathke 1985).
Impacts of slug herbivory
The exclusion of molluscs from plant communities has been shown to have a
marked influence on the survivorship of emerging seedlings. Because seedlings
are more sensitive than adults to the removal of small amounts of tissue, the risk
of mortality due to slugs is highest when the plant is small. Risk is further
enhanced by seedling architecture as slugs more readily attack plants less than
10 cm tall (Albrectsen et al. 2004; Rathke 1985) and find young plants more
palatable than older ones (Fenner et al. 1999). Hulme (1994) followed the fate of
roughly 13,000 seedlings in temperate grassland. Along with rodents, molluscs
were among the most important seedling predators, exploiting on average 30%
3
of all individuals. Less is known regarding slugs’ importance as seedling
predators in forest habitats. In one of the few studies of this kind, Christel et al.
(2002) showed that seedling recruitment of a perennial forest herb in deciduous
forest in Sweden was significantly greater following the application of
molluscicide, and that these effects lasted up to four years following a single
treatment. In open coniferous forest, Nystrand and Grandström (1997)
demonstrated that high densities of the slug Arion subfuscus (Draparnaud)
(Arionidae) were responsible for a three-fold increase in scots pine seedling
mortality.
Though death may not occur, the removal of large amounts of photosynthetic
tissue and the damaging of reproductive organs can reduce the fitness of lowlying adult plants. In a limestone grassland in central England, for example,
Breadmore and Kirk (1998) found that the two slugs Deroceras reticulatum
(Mϋller) (Agriolimacidae) and Arion ater (Linneaus) (Arionidae) were the main
petal herbivores of a wide range of herbaceous plant species, causing damage
exceeding that of arthropods. Mollusc herbivory significantly reduced the number
of capitulae produced by an invasive aster, Senecio inaequidens D.C., despite
the presence of pyrrolizidine alkaloids (Scherber et al. 2003). Rai and Tripathi
(1985) demonstrated that slug and insect herbivory was responsible for delayed
flowering and reduced seed output in the weed Galinsoga quadriradiata Cav.
(Asteraceae).
4
Slugs can have profound effects on single species if they are among their
favored food items. Bruelheide and Scheidel (1999) reported that non-native
slugs removed nearly three-fourths of all leaf tissue from the rare perennial
Arnica montana Linneaus (Asteraceae), and, further, restricted this species to
high elevations where herbivory was less intense. In New Zealand alien slugs
caused extensive defoliation of a native slow-growing fern, thereby facilitating the
invasion of alien plant species (Sessions and Kelley 2002).
Several studies have described the short-term effects of slug grazing in
European pasture, noting a general shift away from the use of highly palatable
herbaceous species towards more herbivore resistant grasses (Wilby and Brown
2001; Hanley et al. 1996). Cates and Orians (1975) found the palatability of 100
species to slugs was strongly correlated with successional status. Annuals were
preferred to perennials and early successional species were preferred to later
successional species, a finding supported by Briner and Frank (1998) using 78
additional plant species. As a result of this work, it has been suggested that
molluscs, and especially slugs, can influence both the rate and direction of
succession.
Slugs in Hawai‘i
According to the plant-defense hypothesis, plants evolve anti-herbivore defenses
in response to grazing (Feeny 1992). Thus, plants that evolved in the presence of
herbivores are likely to be better defended than plants that evolved in their
5
absence. The degree to which plants develop, or fail to develop, herbivore
defenses is largely a function of the combined effects of resource availability and
herbivore pressure (Coley et al. 1985). In an environment with few herbivores,
evolution would tend to favor fast growing, highly fecund individuals over welldefended ones. As a result, when non-native herbivores are introduced into a
plant community, species composition can change rapidly and rare species can
be pushed towards extinction (Coomes et. al 2003; Schreiner 1997). This is a
critical issue in Hawai‘i (Stone 1985), where several important guilds of
herbivores were historically lacking and endemism in the flora and fauna is high
because of the islands’ extreme isolation.
Hawai‘i lacks native slugs, but has a rich native snail fauna (Cowie 1995; Gagné
and Christenson 1985). Native snails have not been reported to eat living plant
tissue; tree snails of the genus Achatinella Swainson (Achatinellidae), for
example, are believed to feed exclusively on epiphytic algae and fungi (Severns
1981; Hadfield and Mountain 1980). The diets of most groups of native snails,
however, have yet to be studied (R. Cowie pers. comm.), and it is therefore
unknown to what extent native plants are adapted to mollusc herbivory. At least
12 slugs and one semi-slug, Parmarion martensi Simroth (Ariophantidae), are
now established in Hawai‘i (Table 1.2). This number is conservative, as thorough
surveys for slugs in Hawai‘i have not been undertaken. While no formal studies
have been conducted to investigate the impacts that alien slugs are having on
native flora, they are nevertheless widely regarded among local botanists to be
6
key limiting factors to native seedling survival and responsible for the failure of
several restoration efforts. The number of endangered Hawaiian plant species
reported by the U.S. Fish and Wildlife Service (USFWS) to be imminently or
potentially threatened by alien slugs is alarming (Table 1.3).
Two field trials in Lyon Arboretum on O‘ahu (A. Yoshinaga, unpublished)
demonstrated that slugs could reduce the survival of Cyanea angustifolia
(Cham.) Hillebr. (Campanulaceae) seedlings by as much as 80%. In one of the
few published reports of slug feeding in Hawai‘i, Gagné (1983) documented the
slug Milax gagates (Draparnaud) (Milacidae) feeding on the native greensword
Argyroxiphium grayanum (Hillebrand) Degener (Asteraceae). Managers with the
Nature Conservancy and the Army Natural Resource Center constructed
elaborate mollusk barriers after plantings of Solanum sandwicense Hook. &
Arnott (Solanaceae), Schiedea kaalae Caum & Hosaka, Schiedea obovata
(Sherff) (Caryophyllaceae), Cyrtandra dentata St. John & Storey and Cyanea
superba (Cham.) A. Gray (Campanulaceae) apparently failed because of slugs
(Sailer 2002; Arcand et al. 2002).
HYPOTHESES
My study investigates the potential impacts of introduced slugs on native and
introduced plants in Hawai’i. The aim of this research is to identify differences (if
any) in plant acceptability to slugs in the laboratory as well as assess the effect of
slug feeding on plant survival and seedling regeneration under natural conditions.
7
Hypotheses specifically addressed are:
H1) The acceptability of plant material to slugs differs among different plant
species
H2) The acceptability of plant material to slugs differs among different slug
species
H3) Slug herbivory is responsible for increased damage to leaf tissue
H4) Slug herbivory is responsible for reduced plant growth
H5) Slug herbivory is responsible for increased seedling mortality
H6) Plant species will differ in the above effects (increased leaf damage, reduced
growth, reduced survival) of slug herbivory
H7) The number and/or species composition of seedlings naturally regenerating
from the seed bank is altered by slug herbivory.
To investigate these hypotheses, two experiments were carried out, one in the
laboratory and one in the field. The first addressed H1 and H2 (Chapter 2) and
was conducted under controlled conditions using five slug species and five plant
species. Plant acceptability was ranked from 0-1 using an index developed by
Dirzo (1980) and differences attributable to slug species, plant species and/or an
interaction between the two, were quantified. A second experiment (Chapter 3)
carried out in the Wai‘anae Mountains, followed the fate of transplanted
seedlings (H3-H6), and tracked changes in the number and identity of germinants
from the seed bank (H7), when exposed to or protected from slug herbivory.
8
TABLES
Table 1.1 Gastropod families containing slugs (South 1992; new family names
from Barker 2001).
Class
Subclass
Order
Familiy
Gastropoda
Gymnomorpha
Soleolifera
Rathouisiidae
Pulmonata
Vaginulidae
Stylommatophora
Urocyclidae
Parmacellidae
Milacidae
Limacidae
Agriolimacidae
Boettgerillidae
Trigonochlamydidae
Arionidae
Philomycidae
9
Table 1.2. List of slugs found within the state of Hawai‘i, island distribution and
year of first record.
Species
Dist. in Hawai‘i
Year first rec.
Native range
Arion distinctus
Mabille
Hawai‘i (D. Foote, pers.
comm.)
2003 (D. Foote,
pers. comm.)
Natural range in Europe
not known (Barker 1999)
A. hortensis
Férussac
Hawai‘i (D. Foote, pers.
comm.)
2003 (D. Foote,
pers. comm.)
Natural range in Europe
not known (Barker 1999)
A. intermedius
Normand
Hawai‘i (Cowie 1999)
1998 (Cowie
1999)
Central and western
Europe (Barker 1999)
Deroceras
leave (Mϋller)
Hawai‘i, Kaua‘i, Maui,
O‘ahu (Cowie 1997)
1897 (Cowie
1997)
Palearctic (Barker 1999)
D. reticulatum
(Mϋller)
Hawai‘i, Kaua‘i (Cowie
1997), O‘ahu (S. Joe pers.
obs.)
1963 (Cowie
1997)
Natural range in Europe
not known (Barker 1999)
Laevicaulis alte
(Férussac)
Hawai‘i, Moloka‘i, O‘ahu
(Cowie 1997)
1900 (Cowie
1997)
Central Africa (Cowie
1997)
Lehmannia
valentiana
(Férussac)
Maui (Cowie 1997), O‘ahu
(S. Joe pers. obs.), Hawai‘i
(D. Foote pers. comm.)
1982 (Cowie
1997)
Iberian Peninsula and
Atlantic Islands (Barker
1999)
Limacus flavus
(Linnaeus)
Maui, O‘ahu (Cowie 1997)
1948 (Cowie
1997)
Natural range in Europe
not known (Barker 1999)
Limax maximus
Linnaeus
Hawai‘i, Maui, O‘ahu
(Cowie 1997)
1931 (Cowie
1997)
Southern and western
Europe (Barker 1999)
Meghimatium
striatum van
Hasselt
Kaua‘i, O‘ahu (Cowie
1997)
1846 (Cowie
1997)
Asia (Cowie 1997)
Milax gagates
(Draparnaud)
Maui, Hawai‘i (Cowie
1997), O‘ahu (Arcand et al.
2002)
1896 (Cowie
1997)
Canary Islands,
Mediterranean and Black
Sea region (Barker 1999)
Parmarion
martensi
Simroth
O‘ahu (Cowie 1997, 1998)
1996 (Cowie
1997)
Cambodia (Cowie 1997)
Sarasinula
plebeia
(Fischer)
Hawai‘i, O‘ahu (Cowie
1997)
1978 (Cowie
1997)
Central and South America
(Rueda et al. 2002)
Veronicella
cubensis
(Pfeiffer)
O‘ahu (Cowie 1997)
1985 (Cowie
1997)
Cuba (Cowie 1997)
10
Table 1.3. List of native species reported by the USFWS to be currently or potentially threatened by alien slugs. Quotation
marks are not used in the comment column, rather, any comments that are not direct quotes but my own interpretation of
the material are enclosed in brackets [].
Species
Family
Comment regarding slugs
Citation
Acaena exigua A. Gray
Rosaceae
.. consumption of vegetative or floral parts of this species by alien
slugs and/or rats could have been a factor in the decline of the
species and could continue to be a critical limiting factor.
USFWS 1997, p.
10
Clermontia oblongifolia
Gaud.
Campanulaceae
[Slugs appear in a table of potential threats to this species.]
USFWS 1997,
Table 1, p. 9
C. samuelii C. Forbes
Campanulaceae
.. slugs (mainly Milax gagetes) are known to eat leaves, stems, and
fruits of other members of this genus, and therefore are a potential
threat.
USFWS 1999, p.
48309
Cyanea Gaud.
Campanulaceae
Little is known about the predation of certain rare Hawaiian plants by
alien snails and slugs. Field botanists have observed slugs preying
indiscriminately on plants belonging to the bellflower family. The
effect of these alien predators on the decline of Cyanea species
(which are in the bellflower family) and related species is unclear,
although slugs may pose a threat by feeding on seedlings, stems,
and fruit, thereby reducing the vigor of the plants and limiting
regeneration.
USFWS 1998c,
pp. 27-28
C. acuminata (Gaud.)
Hillebr.
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. asarifolia St. John
Campanulaceae
Common garden slugs have become widespread in Hawaii and may
pose a major, but little-recognized threat to native plant species.
Slugs can damage flowers, fruits, stems and seedlings of native
plants. Slug damage has been documented on Cyanea asarifolia
and slugs are a potential threat to other Kauai cluster taxa.
USFWS 1995b,
p. 14
C. asplenifolia (Mann)
Hillebr.
Campanulaceae
This species is threatened by ... slugs that directly prey upon and
defoliate the species.
USFWS 2005, p.
24912
11
C. calycina (Cham.)
Lammers
Campanulaceae
Threats to the species include pigs and goats that degrade and
destroy habitat, rats and slugs that directly prey upon it.
USFWS 2005, p.
24880
C. copelandii spp.
haleakalaensis (St.
John) Lammers
Campanulaceae
.. slugs (mainly Milax gagates) are known to eat leaves, stems, and
fruits of other members of this genus, and therefore are a potential
threat to this species.
USFWS 1999, p.
48310
C. crispa (Gaud.)
Lammers, Givnish &
Sytsma
Campanulaceae
The major threats to [this species] are .. suspected predation by ..
slugs.
USFWS 1998c,
p. 57-58
C. dunbariae Rock
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998b,
Table 3, p. 7
C. eleeleensis (St. John)
Lammers
Campanulaceae
This species is highly threatened by ... slugs that eat this plant.
USFWS 2005, p.
24912
C. glabra (F. Wimmer)
St. John
Campanulaceae
Slugs are the primary threat to C. glabra, shown by recent
observations of slug damage on both juveniles and adults.
USFWS 1998b,
p. 11
C. grimesiana
subsp. obatae (St. John)
Lammers
Campanulaceae
The major threats to [this species] are .. predation of seeds or fruits
by introduced slugs.
USFWS 1998c,
p. 59
C. humboldtiana (Gaud.)
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. koolauensis
Lammers, Givnish &
Sytsma
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. kuhihewa Lammers
Campanulaceae
This species is highly threatened by ... slugs that eat this plant.
USFWS 2005, p.
24913
C. kunthiana Hillebr.
Campanulaceae
Slugs have also been observed on C. kunthiana plants, which had
extremely damaged leaves.
USFWS 1998b,
p. 11
C. lanceolata (Gaudich.)
Lammers
Campanulaceae
Threats to the species include pigs, rats, and slugs that prey
upon [it].
USFWS 2005, p.
24880
C. lobata H. Mann
Campanulaceae
[Slugs appear in a table of potential threats to this species.]
USFWS 1997,
12
Table 1, p. 9
C. longiflora (Wawra)
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. mceldowneyi Rock
Campanulaceae
[Slugs appear in a table of potential threats to this species.]
USFWS 1997,
Table 1, p. 9
C. pinnatifida (Cham.) F.
Wimmer
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. tritomantha A. Gray
Campanulaceae
Threats to this species include pigs, rats, and slugs that eat this
plant.
USFWS 2005, p.
24880
C. obtusa (Gray) Hillebr.
Campanulaceae
This species is highly threatened by goats, pigs, cattle, rats,
and slugs that eat this plant.
USFWS 2005, p.
24913
C. recta (Wawra) Hillebr.
Campanulaceae
The major threats to [this species] are .. slugs that feed on the
stems.
USFWS 1998a,
p. 25
C. remyi Rock
Campanulaceae
Reasons for the decline of [this species] are .. slugs that feed on the
stems.
USFWS 1998a,
p. 28
C. st.-johnii
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. superba (Cham.) A.
Gray
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. truncata (Rock) Rock
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. undulata (C. Forbes)
Campanulaceae
Introduced slugs have .. been observed feeding on stems and
leaves.
USFWS 1994, p.
22
Cyrtandra J. R. Forester
& G. Forester
Gesneriaceae
Members of the genus Cyrtandra in the family Gesneriaceae are
also thought to be susceptible to slug predation.
USFWS 1998c,
p. 28
C. crenata St. John &
Storey
Gesneriaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
13
C. dentata St. John &
Storey
Gesneriaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. kaulantha St. John &
Storey
Gesneriaceae
Threats to the species include pigs and slugs that eat this plant.
USFWS 2005, p.
24880
C. polyantha C. B.
Clarke
Gesneriaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. subumbellata
(Hillebr.) St. John &
Storey
Gesneriaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
C. viridiflora St. John &
Storey
Gesneriaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
Delissea rhytidosperrna
H. Mann
Campanulaceae
.. other threats are predation by rats and slugs.
USFWS 1995b,
p. 39
D. subcordata Gaud.
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
Lobelia gaudichaudii
subsp. koolauensis
(Hosaka & Fosb.)
Lammers
Campanulaceae
[Slugs appear in a table of potential threats to this species.]
USFWS 1998c,
Table 3, p. 29
L. monostachya (Rock)
Lammers
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
L. niihauensis St. John
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
L. oahuensis Rock
Campanulaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
Ranunculus hawaiensis
Gray
Ranunculaceae
Threats to the species include competition from nonnative plants,
and damage from slugs.
USFWS 2005, p.
24884
Ranunculus mauiensis
Ranunculaceae
This species is threatened by feral pigs and slugs that eat this plant.
USFWS 2005, p.
24922
14
Schiedea
Ranunculaceae
Based on recent unpublished evidence, recruitment of Schiedea
germinants [seedlings] can be catastrophically suppressed by
herbivory of alien slugs in the Wai‘anae Mountains of O‘ahu.
USFWS 1997, p.
85
Schiedea
Ranunculaceae
There is no evidence of regeneration from seed under field
conditions. Seedlings of species of Schiedea occurring in mesic or
wet sites are apparently consumed by introduced slugs and snails ...
In contrast to mesic-forest species, Schiedea occurring in dry areas
produce abundant seedlings following winter rains, presumably
because there are fewer alien consumers in the drier sites.
USFWS 1998a,
p. 59-60
Schiedea haleakalensis
Caryophyllaceae
[This species] has survived only on precipitous cliff faces
inaccessible to goats. In spite of the removal of goats in the late
1980s from habitat of this taxon in Haleakalā National Park, no
establishment by seedlings has ever been observed. Slugs may be
completely devouring the seedlings.
USFWS 1997, p.
84
S. kaalae Wawra
Caryophyllaceae
This species .. reproduces prolifically under greenhouse conditions.
The lack of seedlings in the field seems, therefore, almost certainly
to be the result of grazing by alien snails and slugs.
USFWS 1998c
S. kauaiensis St. John
Caryophyllaceae
Threats to [this species] include ... predation by introduced slugs.
USFWS 1998a,
p. 60
S. kealiae Caum &
Hosaka
Caryophyllaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
S. membranacea St.
John
Caryophyllaceae
There was no evidence of recruitment in the population, despite the
production of abundant seed during all years of observation (1987,
1994-1997). Introduced snails have been observed feeding on
flowers and developing seed capsules, and garlic snails are
common near the plants. It seems very likely that introduced
molluscs are responsible for the failure of recruitment.
USFWS 1998a,
p. 63
S. stellarioides H. Mann
Caryophyllaceae
[Slugs appear in a table of current threats to this species.]
USFWS 1998c,
Table 3, p. 29
Viola lanaiensis Becker
Violaceae
Slug damage and live slugs have been observed on [this species].
USFWS 1995a,
p. 61
15
CHAPTER 2
PALATABILITY OF FIVE NATIVE HAWAIIAN PLANT SPECIES TO FIVE ALIEN
SLUG SPECIES
INTRODUCTION
Hawai‘i has a very high number of endangered plants, with many species
reduced to small and dwindling populations (Wagner et al. 1999). One of the
most important threats to these disappearing species is predation by introduced
herbivores. Introduced ungulates, for example, have devastated plant
communities in a number of natural areas in Hawai‘i and elsewhere (Coblentz
and Van Vuren 1987; Van Vuren and Coblentz 1987; Stone 1985). Terrestrial
slugs (Mollusca: Pulmonata) are another group of introduced herbivores with no
native representatives in Hawai’i (Cowie 1997). Slugs constitute a polyphyletic
group distinguished from snails by the absence of an external shell (Runham and
Hunter 1970). They are important seedling predators in native (Wilby and Brown
2001; Hulme 1994) and introduced habitats (Ferguson 2004; Fritz et al. 2001) in
many parts of the world. In Hawai‘i, there is copious anecdotal information
suggesting that they harm native plants yet, to date, they have been the focus of
little research.
Theories of plant defense evolution hinge on the assumption that the resistance
conferred by defense mechanisms involves an allocation of resources which, in
the absence of herbivores, could be put towards other fitness-enhancing ends
16
(Coley et al. 1985). Plant defense mechanisms include structural defenses like
spines or hairs that can interfere with feeding (Pollard 1992), as well as chemical
defenses in the form of secondary compounds that can influence plant
palatability or digestibility (Arnold 1980). Although the cost of defense is not
always obvious (Siemens et al. 2002), a recent synthesis of 33 studies supports
the idea of inherent trade-offs between allocation to plant defense and other
fitness-enhancing activities such as growth and reproduction (Strauss et al.
2002). Because Hawaiian plants evolved in the absence of slugs, it could be
hypothesized that most native plants will be highly vulnerable to slug herbivory
due to the loss of unnecessary defense mechanisms and hence increased
palatability. In the Santa Cruz Islands, for example, Bowen and Van Vuren
(1997) found higher acceptability to domestic sheep and lower chemical
defenses in plant species relative to mainland congenerics. But Hawaiian plants
have had to defend themselves against arthropod and avian herbivores (Givnish
et al. 1994), and some of the mechanisms that protect them from these
consumers may also be effective against novel ones. In addition, phylogenetic
inertia may dictate that certain groups of native plants use different defenses, or
retain them for longer periods of evolutionary time, than others. It has long been
recognized, for example, that introduced ungulates prefer certain native plants to
others (Scowcroft and Giffin 1983) suggesting rejected species may have
retained defenses. Likewise, native Hawaiian plants may not be equally attractive
to alien slugs, and further, food preferences may differ among different slug
species.
17
Variability in the feeding relationships between native plants and alien slugs
should have important implications for conservation in Hawai’i. Knowledge of
which plant species are most palatable, and which slug species are most likely to
eat them, will allow more informed management decisions regarding the
protection and restoration of endangered plant populations. As a first effort to
establish this base of information, I investigated five endangered plant species
and five introduced slug species, and used relative acceptability indices (Dirzo
1980) to assess whether there are differences among these taxa in either
palatability or feeding preference.
MATERIALS AND METHODS
Study organisms
Cyanea Gaud. (Campanulaceae), the largest genus of plants endemic to the
Hawaiian archipelago, once contained 52 species, of which 14 are now extinct
and 15 are listed as endangered by the U.S. federal government (Wagner et al.
1999). Slugs have been observed to eat the leaves, stems and fruits of many
Cyanea species (Chapter 1) and are suspected of contributing to their decline.
Cyanea grimesiana Gaud. ssp. obatae (St. John) Lammers is a shrub, usually
unbranched, 1-3.2 m in height, typically found on steep, moist, shaded slopes in
diverse mesic to wet forests between 550 and 670 m elevation (Wagner et al.
1999). Endemic to the Wai‘anae Mountains on the island of O‘ahu, only 13
individuals of this subspecies remain in the wild (USFWS 1998c).
18
Brighamia A. Gray, also in the Campanulaceae, contains two species, both
endangered. Brighamia rockii St. John is a stout unbranched succulent, 1-5 m
tall, currently restricted to steep, inaccessible sea cliffs along East Moloka‘i’s
northern coastline between sea level and 470 m elevation (Wagner et al. 1999).
Fewer than 200 plants occur in the wild (USFWS 1996). Slugs may not be a
serious concern for this species if they do not forage on sea cliffs. Nonetheless,
this plant may have had a broader habitat range in the past, and introduced slugs
could have played a role in restricting its range. Slugs readily consume plants
grown under greenhouse conditions and are known to kill adult plants by
burrowing into the fleshy stem and hollowing out the center (M. Sherman pers.
comm.; K. Swift pers. comm.).
Slugs have been observed to feed readily on a number of species of Scheidea
Cham. & Schlechtend., non A. Rich. nec Bartl (Chapter 1), a speciose endemic
genus. Scheidea obovata (Sherff) (Caryophyllaceae) is a branching subshrub
attaining heights of approximately 1 m and possessing thick, fleshy, deep green
leaves that are either opposite or whorled about the stem. This species occurs in
diverse mesic forest from 550 to 800 m elevation on ridges and slopes in the
Wai‘anae Mountains (Wagner et al. 1999). In 1994, the three known wild
populations contained 11 individuals in total (USFWS 1994).
Urera kaalae Wawra (Urticaceae) is a small tree, 3-7 m tall, with distinctive
greenish sap that turns black when exposed to the air and has thin, heart19
shaped, pale green leaves, serrate at their margins (Wagner et al. 1999).
Endemic to the Wai‘anae Mountains, this species grows on slopes and gulches
in diverse mesic forest at elevations of 300-820 m. About a decade ago, an
estimated 40 plants remained in the wild (USFWS 1994). In an effort to prevent
further decline, the Nature Conservancy has been augmenting natural
populations with greenhouse seedlings but reports that slug predation of these
plants is high (Sailer 2002).
Solanum sandwicense Hook & Arnott (Solanaceae) is a shrub, 4-5 m tall, with
simple unarmed leaves, occurring in diverse mesic forest between 760 and 1220
m elevation on O‘ahu and Kaua‘i. Young parts are densely pubescent and
reddish pubescence coats the underside of the leaves (Wagner et al. 1999). The
O‘ahu population, which in 1995 shrank to one plant (USFWS 1995b), now
numbers about 10 thanks to captive propagation and outplanting of seedlings by
Nature Conservancy staff.
The five slug species used in the present study are among the most common on
O‘ahu, and at least three of them co-occur with the plant species tested here.
Between 30 and 80 slugs of each species were collected between May and June
2003 from two areas on O‘ahu: at 700 m elevation in the Kahanahāiki
Management Unit (KMU), a preserve managed by the U.S. Army in the northern
Wai‘anae Mountains; and at 60 m elevation in the Kaimuki residential district of
Honolulu (Figure 2.1). Due to an apparent stratification in the distribution of these
20
slugs, the two veronicellid species: Laevicaulis alte (Férussac) and Veronicella
cubensis (Pfeiffer) were more common at elevations < 300 m, in residential
areas, while the other three, Limax maximus Linnaeus (Limacidae), Limacus
flavus (Linnaeus) (Limacidae), and Meghimatium striatum van Hasselt
(Phylomicidae) were more common in forested areas > 300 m (S. Joe pers.
obs.). Despite these differences, all species survived well in Kaimuki, where they
were housed outdoors in the shade and exposed to natural weather and light
conditions through February 2004, after which they were killed.
Feeding trial protocol
Following capture, each slug was weighed and housed in a single 266 ml plastic
cup containing a substrate of fine cinder 5 cm deep. A mesh top secured by a
rubber band prevented escape. Holes punched into the bottom of the cups
allowed for water drainage and a wet cloth placed over the top prevented
dehydration. Study slugs probably included both juveniles and adults, as maturity
was not confirmed prior to the feeding trials. Species identifications were made
using external morphology.
Slugs can remember unacceptable food for up to three weeks after a single
encounter (Gelperin 1975); therefore, an interval of at least three weeks was
allowed between feeding trials. In the intervals, slugs received a diet of Beneful
® (Nestlé Purina PetCare Company, St. Louis, Missouri, USA) dog kibble and
Aloha brand (Aloha Seed & Herb Paia, Hawai’i, USA) buttercrunch lettuce
21
(Lactuca sativa L.). Palatability testing began in August 2003 and ended 6
months later.
An acceptability index (AI) was used to measure plant palatability (Dirzo 1980).
On the day of testing, each slug was weighed, placed in a fresh cup containing
only moistened filter paper and a pair of 15 cm2 leaf discs, one from the test
species and one from a highly acceptable control species, in this case, lettuce,
and allowed to feed for 48 hours, after which they were returned to their original
cups. Although Dirzo (1980) allowed slugs to feed for only 12 hours, they were
starved 24 hours prior to testing. In order to reduce the labor required to transfer
slugs into new containers, slugs were not starved prior to testing as in Dirzo
(1980). Instead the duration of each trail was increased. Uniformity of disc size
was maintained using a hole puncher, and measurement of the leaf surface area
both before and after slug feeding was made with a LI-3000A Portable Area
Meter (LI-COR Environmental, Lincoln, Nebraska USA). The index was
calculated as the area eaten from the test species leaf disc divided by that eaten
from the lettuce disc. Thus, in order for a trial to be considered valid, some or all
of the lettuce disc must be consumed by the slug. Instances in which the slug ate
neither disc were discounted, along with instances in which the slug ate only the
test disc. Multiple test plant species were then ranked by relative palatability
according to their AI scores. AI scores have the benefit of controlling for slug size
since the ratio remains the same for a small slug eating a small amount of food
and a larger slug eating a large amount.
22
All plants with the exception of B. rockii, which came from the Hui Ku Maoli Ola
Native Hawaiian Plant Nursery in Waimanalo, O‘ahu, and lettuce, which was
grown by myself from seed, were borrowed from the Nature Conservancy’s rare
plant nursery in Wahiawa. Plant age can affect palatability (Fenner et al. 1999);
thus I only harvested mature leaves from adult (i.e. reproductive) plants for use in
feeding trials. No more than three plants per species (not including lettuce, which
came from approximately 12 plants) served as leaf disc donors because of their
extreme rarity. Intraspecific variation in plant palatability, if it exists, was not
addressed in this study. After feeding trials had concluded, plants were returned
to the Wahiawa nursery for use in restoration projects. None died as a result of
leaf harvesting.
Because test plant material was limited to a one-time harvest, it was necessary
to present each plant species to all slugs on a single occasion rather than
randomizing the order of plant presentation for each slug. Thus, the order of plant
species presentation, determined randomly, and commencing on the date in
parentheses, was as follows: C. grimesiana ssp. obatae (27 August 2003), S.
sandwicense (27 September 2003), U. kaalae (31 October 2003), B. rockii (26
November 2003), and S. obovata (28 December 2003). Because of the long
interval between feeding trials, some slugs died before being offering all five
plant species. Because these were not replaced, there was a very slight attrition
in slug number over the study period. Mortality did not exceed two slugs per
23
species, a remarkably low number considering reported losses of greater than
50% over three weeks for other studies of this type (Gebauer 2002; Glen et al.
2000; Wilson et al. 1999).
Statistical Analysis
Because slug size was expected to differ among species, differences in slug
weights were analyzed using a one-way ANOVA. The effects of plant species,
slug species, and plant x slug interaction on AI scores were analyzed with a twoway ANOVA, with all factors fixed. The AI scores did not meet all the
assumptions of ANOVA, that is, residuals were not normally distributed and were
heteroscedastic. However, variances among the different groups were not
significantly different (Levene’s Test; P=0.243). Log transformation of the data
yielded results almost identical to those of the untransformed data and did not
improve the distribution of the model’s residuals. I judged that this violation of
residual normality was preferable to using a combination of tests on subsets of
the data. All statistical analyses were performed with Minitab® Release 14
software (Ryan et al. 2005).
RESULTS
Feeding activity was low during each of the five trials regardless of slug species,
with, on average, only one in every five slugs feeding (Fig. 2.2). This allowed
estimation of AI scores based on sample sizes ranging from four to 20 AI
replicates for each slug\plant species pair (Table 2.1). An AI of 0 indicates
24
complete rejection of the test species. A two-way ANOVA identified a significant
difference in palatability among plant species, but no statistical difference in
overall feeding among slug species, and no plant-by-slug species interaction
(Table 2.2). Post-hoc testing indicated that palatability differences among plant
species were significant (Tukey’s HSD) only between U. kaalae and the other
four plant species, with U. kaalae being more palatable than the other species
(Figure 2.3). The high frequency of AI scores close to zero (Figure 2.4) shows
most of the test plant species offered to slugs were rejected and were not nearly
as acceptable as the control.
As expected, slug taxa differed significantly by weight (one-way ANOVA;
F=42.23; P<0.0001), with groups differing at the family level (Figure 2.5). The two
limacid species were heaviest, followed by the two veronicellids in the midrange
and M. striatum the lightest of the group.
DISCUSSION
The results of this experiment indicate that there is significant variation in
palatability among native Hawaiian plants, with U. kaalae significantly more
palatable than the other four plant species tested. Urera kaalae was considerably
more palatable, even, than the two Campanulaceae species (C. grimesiana and
B. rockii), a plant family previously noted to be especially attractive to slugs in
Hawai‘i (Sailer 2002).
25
Somewhat surprisingly, there was no significant difference among slug species in
food preference. This may reflect similarities these slugs share as colonizing
species, such as non-specialist feeding behavior stemming from the absence of
tightly co-evolved relationships with local plants. Alternatively, small sample
sizes, combined with high variation among trials, may have obscured more subtle
differences in plant preference among the slug species.
Even though I started with relatively large numbers of slug replicates, the majority
of trials resulted in no feeding and had to be discounted. While failure to eat
caused many trails to be omitted from analysis, no omissions occurred as a
result of slugs eating the test plant but not the control. In order to account for this
possibility, others (Kelly and Hanley 2005) have calculated AI from the area of
the test disc eaten divided by the area of both discs eaten. Feeding might have
been observed in a greater proportion of trails by starving the slugs for a period
of time prior to testing or by increasing the length of each trail to more than 48
hours. Gebauer (2002), for example, exposed test foods to slugs for 7 days. In
addition, I suspect the slugs were overfed prior to and in between testing, as all
gained weight and continued to gain weight during their months in captivity.
Perhaps more importantly, the data reveal large variation in feeding preferences
by individual slugs. For example, a single L. flavus ate 31 times more U. kaalae
than lettuce, but failed to eat anything in any of the other trials. To a lesser
degree, other individual slugs showed distinct preferences that may, or may not,
have been in line with the average for their species. Other studies have typically
26
dealt with this problem by omitting “anomalous” (Brooks et al. 2003) or “deviant”
(Dirzo 1980) slugs from the analysis. The frequency of such behavior, however,
imply that while there may be valid preferences for a slug species as a whole,
there is a lot of meaningful intraspecific variation that should be recognized.
The distribution of AI scores close to 0 (Figure 2.5) was similar to that observed
by Dirzo (1980) who found that slugs rejected, on average, 42% of the 30 plant
species offered. He went on to characterize slug food preferences as falling
within one of the following three categories: rejected or rarely chosen, moderately
acceptable and very acceptable. Why so many species were rejected for rarely
chosen remains the subject of much speculation. Slugs have complex feeding
behavior. Food choice is driven not only by metabolic requirements and plant
defenses, but is also subject to more subtle influences such as the prior
experience of the animal (Gouyon et al. 1983). It has been demonstrated, for
example, that the slug Limax maximus is capable of associative learning that
subsequently guides its food choices (Sahley et al. 1981). Food preferences
among slugs are not static, and depend in part upon the availability of other
foods and the frequency with which they are encountered. Slugs often prefer
novel foods over familiar ones (Cottam 1985; Mølgaard 1986a), and may
consume up to 270% more when offered a choice of foods (Peters et al. 2000).
This behavior has been described as “neophilic” by some authors (Cook et al.
2000) and even extends to foods that are known to contain noxious compounds.
Slugs tend to eat such foods too, at least until the novelty wears off (Whelan
27
1982). Thus, a rare plant may be more likely to be attacked by slugs just by virtue
of being rare.
The level of risk incurred by a native plant will largely depend on how palatable it
is relative to other available plants. Unfortunately, few of these neighbors are
likely to be lettuce. Though S. obovata had the lowest mean acceptability among
the species tested, the area where it occurs is dominated by invasive strawberry
guava, Psidium cattleianum Sabine. Herbivore damage to P. cattleianum in the
field is negligible (S. Joe pers. obs.). Leaf extracts from Psidium guajava (L.), a
related species, contain biologically active chemical compounds which can have
an analgesic effect (Somchit et al. 2004) and disrupt reproduction in mammals
(Lapçik et al. 2005) and these may have strong anti-herbivory properties.
Whether seedling tissue in my test species is more acceptable to slugs than adult
tissue, something that has been found to be true for other species (Fenner et al.
1999), remains unknown; however, anecdotal reports suggest that adult plant
parts are vulnerable as well (see Study Organisms Materials and Methods).
Because of the rarity of plant species tested, and because the harvesting of
seedling tissue would require the destruction of plants, only adult tissue was
used in the present study. In order to explore differences in adult and seedling
palatability, future studies should draw from a pool of non-endangered plant
species the seedlings of which can be sacrificed.
28
The complex behavior of slugs and the variation in plant community composition
make it difficult to extend results from lab-based preference trials to feeding
behavior in nature. At the least, this study suggests that all five of the native
species tested are likely to be fed upon to some degree in nature. It also
identifies U. kaalae as a species that may be exceedingly vulnerable to slug
herbivory. The predictive power of palatability trials such as this one, however,
could be strengthened if correlated on a broad scale with plant defense
structures and species-specific secondary compound content. For example,
pubescence has been shown to deter slug herbivory in some plant species
(Westerbergh and Nyberg 1995). The pubescence on S. sandwicense may have
reduced its acceptability, but it clearly did not prevent slug feeding entirely. A
number of secondary compounds are also known to deter slug herbivory (Table
2.3). Swanholm et al. (1959; 1960) found alkaloids in a significant number of
Hawaiian plants in various families, including the Campanulaceae species
Cyanea angustifolia and Clermontia kakeana. Despite this finding, the two
Campanulaceae species were eaten by slugs in this study, and Cyanea suberba
is heavily fed upon by slugs in field trials (Chapter 3). It may be that these
alkaloids are not especially effective in deterring slug herbivory, or there may be
large intrafamilial or even intrageneric differences in chemical content. With
additional research, some of these questions could be resolved.
29
TABLES
Table 2.1. Mean acceptability indices (AI) for 25 slug-plant species pairs. N
equals the number of slugs that consumed any part of one or both leaf discs. In
order for a plant species to be completely rejected (AI=0) all or a portion of the
lettuce must have been consumed.
Slug species
Plant species
N
AI
sd ±
Laevicaulis alte
Brighamia rockii
9
0.43203
0.9157
Cyanea grimesiana
16
0.39834
0.5158
Schiedea obovata
7
0
0
Solanum sandwicense
16
0.09772
0.1614
Urera kaalae
13
1.08496
1.1489
Brighamia rockii
9
0.28909
0.8673
Cyanea grimesiana
7
0.04579
0.0682
Schiedea obovata
9
0
0
Solanum sandwicense
8
0.24592
0.3174
Urera kaalae
10
3.74690
10.3447
Brighamia rockii
7
0
0
Cyanea grimesiana
9
0.08891
0.1077
Schiedea obovata
6
0
0
Solanum sandwicense
14
0.36335
0.4483
Urera kaalae
10
0.34475
0.4437
Brighamia rockii
17
0
0
Cyanea grimesiana
10
0.14383
0.3247
Schiedea obovata
20
0.223947
0.7341
Solanum sandwicense
15
0.07970
0.1109
Urera kaalae
16
0.28902
0.8327
Brighamia rockii
7
0.60608
0.3270
Cyanea grimesiana
4
0.13342
0.2203
Schiedea obovata
6
0.03685
0.0824
Solanum sandwicense
8
0.17355
0.1434
Urera kaalae
7
1.77946
1.0605
Limacus flavus
Limax maximus
Meghimatium striatum
Veronicella cubensis
30
Table 2.2. ANOVA using AI scores from 25 slug-plant species pairs.
Source of
variation
Adj MS
df
F-ratio
P
Slug species
4.127
4
1.03
0.391
Plant
species
16.236
4
4.06
0.003
Slug x plant
species
4.275
16
1.07
0.386
Error
4
231
Table 2.3. Secondary plant compounds repellent to slugs.
Slug
Plant
Repellent
Reference
Arion subfuscus
Salix eriocephala
condensed tannins
Albrectsen et al. 2004
Deroceras reticulatum
Conium maculatum,
Coriandrum sativum,
Petroselinum crispum
alkaloids
Birkett et al. 2004
Deroceras reticulatum
Trifolium repens
cyanogenic
glycosides
Raffaelli and Mordue
1990
Deroceras reticulatum
Arion ater
Plantago major ssp.
pleiosperma
caffeic acids
Mølgaard 1986b
Deroceras reticulatum
Thymus vulgaris
monoterpenes
Gouyon et al. 1983
31
FIGURES
Figure 2.1. Slug collection sites. Laevicaulis alte and Veronicella cubensis were
collected in Kaimuki, while the remainder were collected in Kahanahāiki
Management Unit, a forested area managed by the U.S. Army in the Wai‘anae
Mountains.
32
Figure 2.2. Percent of slugs (bars are one SEM) engaged in feeding (i.e. ate all or a portion of the control species),
averaged among five feeding trials.
33
Figure 2.3. Mean AI scores (bars are one SEM) for each plant species (all slug species pooled). The asterisk (*) indicates
that this group differs significantly (P<0.05) from the rest (Tukey’s HSD).
34
Figure 2.4. Distribution of AI scores (all slug species and plants combined) (single data point of AI = ~31 not shown).
35
Figure 2.5. Boxplot showing weight distribution of slug species. Outliers are marked with asterisks (*). Circles indicate
means.
36
CHAPTER 3
IMPACT OF ALIEN SLUGS ON NATIVE PLANT SEEDLINGS IN A DIVERSE
MESIC FOREST, O‘AHU, HAWAI‘I
INTRODUCTION
Plant seedling survival in a natural environment depends on a number of factors,
including growth rate, level of competition for light and nutrients, and the
magnitude of herbivory. The relative rate of seedling survival among species, in
turn, is a key factor influencing the composition of a plant community (Fritz et al.
2001, Buckland and Grime 2000). Herbivores that target seedlings, therefore,
affect not only individual plants and plant species, but also influence the make-up
of mature plant assemblages. In response to herbivory, plants often protect their
seedlings using defense mechanisms, such as the production of secondary
compounds that deter feeding. This evolutionary interplay between plants and
seedling herbivores is a central dynamic shaping biotic communities. It follows
that the introduction of novel herbivores may have profound consequences that
reverberate throughout the community.
Slugs are generalist herbivores (Rathke 1985) that feed principally on plant
seedlings and low-lying herbs, yet they are not completely indiscriminate in their
choices of foods (Dirzo 1980). In their native ranges, slugs and other molluscs
are known to be important herbivores that influence seedling survival and plant
community species composition. In European grasslands, molluscs, and
37
especially slugs, affect seedling survival (Hulme 1994), shift relative abundances
of palatable versus resistant species (Hanley et al. 1996; Wilby and Brown 2001),
and may influence both the rate and direction of plant succession (Briner and
Frank 1998, Cates and Orians 1975). In forest habitats, Christel et al. (2002),
found that seedling recruitment of a perennial forest herb was significantly
greater following application of molluscicide, and Nystrand and Grandström
(1997) demonstrated that high densities of the slug Arion subfuscus (Drap.) were
responsible for a three-fold increase in Scots pine seedling mortality. Even
among low-statured adult plants, the removal of large amounts of photosynthetic
tissue and the damaging of reproductive organs by slugs can reduce plant fitness
(Scherber et al. 2003, Breadmore and Kirk 1998, Rai and Tripathi 1985).
Hawai‘i has no native slugs, but has a rich native snail fauna (Cowie 1995;
Gagné and Christenson 1985). Native snails in the Achatinellidae and
Amastridae are thought to eat decaying plant material and fungus (Severns
1981; Hadfield and Mountain 1980). Outside these families, little is known
regarding the feeding behavior of native snails (Cowie pers. comm.).
Nonetheless, there is presently no evidence that native snails eat live vascular
plants. The dozen or more species of slugs now established in Hawai’i (Chapter
1), therefore, may represent an entirely new guild of herbivores. Although native
Hawaiian plants have had to defend themselves against avian, insect and
possibly snail herbivory, the defense mechanisms evolved by Hawaiian plants
may not be very effective against introduced slugs. Slugs, in fact, are widely
38
regarded by local botanists as key limiting factors in native seedling survival,
especially among the Campanulaceae, and are believed to be responsible for the
failure of restoration efforts (Chapter 1). Detailed research of these impacts in
Hawai‘i, however, is lacking.
Because of their ability to shift plant species composition through selective
feeding, slugs could serve as an important pressure favoring alien plants over
native species. In New Zealand, for example, alien slugs caused extensive
defoliation in a slow-growing native fern, thereby facilitating the invasion of alien
plant species (Sessions and Kelley 2002). In Hawai‘i, slugs were found to prefer
certain native plants over others (Chapter 2), and, for the following reasons, it
seems likely that palatability asymmetries will be magnified with respect to
naturalized alien plants. Most introduced plant species have evolved with slugs,
and may therefore be better-defended and less palatable, in general, than their
now sympatric native competitors. Although other factors, such as life history
traits, will influence competitive outcomes between native and alien plant
species, seedling herbivory by slugs may be important.
I used a replicated experimental design to investigate the effects of slug
herbivory on native and alien seedling growth and survival in a natural field
setting on O‘ahu, Hawai‘i. I chose three native and two alien plant species that
occur at the field site, and measured plant growth, degree of feeding damage
and overall survival of outplanted seedlings in slug-accessible and slug-free
39
plots. I also monitored natural plant germination and growth from the seed bank
in the replicated plots. Finally, I monitored slug species composition and
abundance over the course of the six-month study in order to document ambient
slug population levels at this site.
MATERIALS AND METHODS
Field Site
Slugs are believed to be major seedling predators of several rare and
endangered plant species on military land in Hawai‘i under management by the
U.S. Army Garrison Natural Resources Division (AGNRD) (Arcand et al. 2002).
Of particular biological significance are areas encompassed by the Kahanahāiki
Management Unit (KMU), which was therefore chosen for this study. KMU is
situated at 700 m elevation on the northeast rim of Mākua Valley, in the Wai‘anae
Mountains on the island of O‘ahu (Figure. 3.1). This area is classified as Montane
Diverse Mesic Forest (Gagné and Cuddily 1999) as it receives approximately
3000 mm of rainfall annually (Arcand et al. 2002).
The KMU harbors 12 endangered plant species, two endangered animal species
and is the site of the first endangered species restoration effort by the military in
Hawai‘i. In consequence, AGNRD staff have taken steps to minimize damage
from alien ungulates have been taken, including the construction of a fence in
1996 and the removal of feral goats and pigs within the fenced enclosure.
Rodents are controlled using snap traps and bait stations arranged in a grid
40
throughout the enclosure. Such activities are important to the present study as
they reduce the level of herbivory and plant deaths not attributable to slugs.
The predominant canopy tree is the alien Psidium cattleianum Sabine
(Myrtaceae), followed by another invasive tree, Schinus terebinthifolius Raddi
(Anacardiaceae). Also common is a Polynesian introduction, Aleurites moluccana
(L.) Willd (Euphorbiaceae). While approximately 90% of the canopy is dominated
by these introduced species, the remainder consists mainly of native trees (S.
Joe pers. obs.). Most frequently encountered are Acacia koa A. Gray (Fabaceae)
and Metrosideros polymorpha Gaud. (Myrtaceae), followed by Pisonia
brunoniana Endl. (Nyctaginaceae) and Nestegis sandwicensis (Gray) O.& I. Deg.
& L. Johnson (Oleaceae). Other, less common trees include Charpentiera
obovata Gaud. (Amaranthaceae) and Pouteria sandwicensis (Gray) Baehni & O.
Deg. (Sapotaceae). Common understory plants include the invasive species
Clidemia hirta (L.) D. Don (Melastomataceae) and Rubus argutus Link
(Rosaceae), interspersed with native species of Hedyotis L. (Rubiaceae) and
Melicope (J.R. & G. Forst.) T.G. Hartley & B.C. Stone (Rutaceae). Natural
populations of endangered natives occur throughout the area, including Cyanea
superba (Cham.) A. Gray (Campanulaceae) and Schiedea obovata (Sherff)
(Caryophillaceae), which are augmented annually with greenhouse reared
individuals.
41
With the assistance of five AGNRD staff, I conducted daytime searches for slugs
on three separate occasions in August 2003. Searches began at 1:00 PM and
ended at 2:00 PM. Through these surveys, I confirmed the presence of at least
four slug species at KMU (S. Joe pers. obs.), listed here from most to least
common: Deroceras Rafinesque sp. (Agriolimacidae), Limax maximus Linnaeus
(Limacidae), Meghimatium striatum van Hasselt (Philomycidae) and Limacus
flavus (Linnaeus) (Limacidae).
Study species
Three native (Cyanea superba, Schiedea obovata and Nestegis sandwicensis)
and two alien (Clidemia hirta and Psidium cattleianum) species were chosen for
the seedling growth and survival experiment. Cyanea superba is a palm-like tree
reaching heights of 4-6 m when mature. Although two subspecies of C. superba
are recognized, I do not distinguish them here because one of them C. superba
regina (Wawra) Lammers has not been collected since 1932, and is likely
extirpated (Wagner et al. 1999) and was not known from the Wai‘anae
Mountains. The remaining extant subspecies, C. superba superba, is referred to
throughout this paper simply as C. superba. After its collection in 1870, there
were no further documented sightings of C. superba until its rediscovery in the
Wai‘anae Mountains in 1971 (Wagner et al. 1999). Presently it is known from
only one small population in the KMU, which, in 1998, numbered only 5 plants
(USFWS 1998c). Schiedea obovata, is a branching shrub growing to 3-10 dm
height. Historically, S. obovata was found throughout the Wai’anae mountain
42
range scattered on ridges and slopes in diverse mesic forest, at elevations of
550-800 m (Wagner et al. 1999). Currently, the KMU is one of only three sites
were S. obovata can be found. As of 2000, the total number of plants was
estimated to be about 30 (Arcand et al. 2002). Nestegis sandwicensis is an
endemic tree 8-25 m tall found in dry to mesic forest on all of the main Hawaiian
islands (except Ni‘ihau) (Wagner et al. 1999). It is locally common in the KMU
where it serves as the plant host to native snails in the genus Achatinella (Arcand
et al. 2002). Both C. hirta and P. cattleianum are highly invasive weeds native to
Central and South America. In Hawai‘i, they form dense, monotypic stands in
mesic to wet areas at 10-1500 m elevation. Clidemia hirta is a perennial shrub
0.5-3 m tall, while P. cattleianum is a short tree 2-6 m tall.
Seedling preparation
Schiedea obovata and C. superba were grown from seed by AGNRD staff at the
Hawai‘i Department of Land and Natural Resources (DLNR) Native Plant Nursery
adjacent to the KMU and located in the Wai‘anae Mountains at an elevation of
700 m. One month prior to planting, plants were moved on site but remained in
pots elevated on flats to prevent slug predation. At this time seedlings from C.
hirta, N. sandwicensis and P. cattleianum, all abundant on site, were dug up,
planted into pots and moved onto flats. Plants were selected by size, number of
leaves (2-4) and absence of any herbivore damage. Height and number of
seedlings by species is given in Table 3.1. In an effort to maximize survival
43
among native plant species, these were planted at larger sizes than either C.
hirta or P. cattleianum.
Experimental design
Thirty 1 m2 plots were established along a contour close to the Kahanahāiki
gulch bottom in February of 2004. Plots fell within an area roughly 0.6 ha, but
random placement within this area was impossible due a steep slope and
presence of dense stands of P. cattleianum. Instead, plots were arranged
wherever trees did not interfere with placement, the slope was less than 35˚ and
the nearest plot was at least 5 m away. Half of these plots (n = 15) were then
randomly selected to receive physical and chemical barriers to slugs, while the
remainder were exposed to natural levels of slug herbivory. In this paper, I refer
to the former as the ‘slug-excluded’ treatment and the latter as the ‘slug-exposed’
treatment.
A copper mesh fence 15 cm high, buried to a depth of 5 cm and topped with a 5
cm strip of zinc tape enclosed all slug-excluded plots to prevent incursion of new
slugs. For the slug-exposed treatment, a galvanized steel mesh fence of similar
dimensions enclosed the plots, but 5 X 5 cm holes were cut into the bottom at 10
cm intervals to allow entry by slugs. Both the copper and galvanized steel
hardware cloth were purchased from TWP Wire Mesh Inc. Berkeley, CA, had
wire diameters of 0.71 mm and a mesh density of 3 squares per cm. Zinc tape
was purchased from BAC Corrosion Control Ltd. (Telford, UK). While copper
44
barriers are known to repel slugs better than those constructed of other materials
(Hata et al. 1997), the effect is enhanced when copper is combined with zinc (S.
Joe unpub. data). In order to test the efficacy of this method I recorded the length
of time it took for a slug to cross a line of tape 5 cm wide laid in a circle with the
slug at its center. Circle boundaries were delineated using zinc and copper tape
alone and in combination or masking tape (the control). Slugs were encouraged
to escape the circle by shining a bright desk lamp on them. All slugs succeeded
in escaping the control, the zinc and the copper circles within 5 minutes. In
contrast, 80% of L. maximus (n = 30), 60% of L. flavus (n = 10) and 10% of M.
striatum (n = 20) failed to cross a combination zinc/copper barrier within 5
minutes. Why some species were more sensitive than others is not known, but
may be due to differences in mucosal conductivity.
A waterproof bait station containing the molluscicide Corry’s Slug and Snail
Death® (Corry & Co. Limited, North Bend, Washington, USA) was placed at the
center of each slug-excluded plot to eliminate any slugs that managed to breach
the barrier as well as any pre-existing, resident slugs. Bait was replenished every
20 days. Empty bait stations were placed at the centers of slug-exposed plots.
All plots were cleared of pre-existing vegetation and raked. Each plot was split in
half; one half received transplanted seedlings (S. obovata (n = 3), N.
sandwicensis (n = 3), C. superba (n = 5), C. hirta (n = 5) and P. cattleianum (n =
5) and the other was left fallow and natural germination from the seed bank was
45
monitored. In the half of the plots receiving seedlings, species were arranged
randomly in 3 columns of 7 plants. Columns were spaced 8.3 cm apart and
plants within each column were spaced 7.1 cm from one another. With
assistance from AGNRD staff, all seedlings were planted on 23 February 2004
and monitored through 1 September 2004, for a total of 190 days. Whereas
growth and survival of transplanted seedlings were recorded approximately every
10 days, natural regeneration was assessed only once at the end of the study.
This was because very few seedlings in total germinated in the cleared plots and,
thus, were easily counted and identified. Germinants coming up among the
transplanted seedlings were pulled to prevent crowding, however this was rarely
necessary as very few were found. These were noted but not included in the
counts of seedlings regenerating from the fallow half of the plot. Each plot
received 1.9 L of water every 10 days to minimize transplant losses and to
encourage germination from the seed bank in the fallow side of the plot.
The following measurements were recorded for transplanted seedlings.
1. Survival status. If dead, no further data were recorded.
2. Number of leaves.
3. Herbivore damage. This was the proportion of leaf removed. Damage
categories were: 0 or no damage, 1-25%, 26-50%, 51-75%, 76-95%.
4. Discoloration and senescence of the leaves caused by disease and/or
nutrient deficiency , were noted but not quantified.
46
5. Plant growth. An index of overall plant size, in dm3, was calculated based
on the formula for a cylinder (V = π r2 h ) where h is plant height and r is
length of the longest leaf.
Slug monitoring
Slug species composition and abundance were assessed using a total of 30
simple refugium traps consisting of 1 m2 pieces of unwaxed cardboard (Hawkins
et al.1998) placed on the ground within 1 m of each study plot. The traps
degraded quickly, so they were replaced once a month following a count of slugs
on top of or underneath the cardboard square. The use of traps to estimate
population densities can yield biased results. Compared to absolute sampling
methods, such as hand searching of soil and litter samples, large slug species
tend to be over-represented and small slug species (< 3.5 mm) underrepresented
(McCoy 1999). This is presumably because larger slugs can travel greater
distances and are therefore more likely to find the refugia. However, the traps
should provide fairly accurate information, within slug species, about relative
abundances across space and time. This relative abundance information was
used to assess uniformity of slug abundance among the plots and to provide
information on slug population fluctuation throughout the study period.
Statistical analysis
At the end of 190 days, seedling measurements were averaged for all individuals
of each species in each plot, because conspecific individuals in the same plot
47
should not be treated as being independent. If no representatives of a given
species remained within the plot, it was omitted from the analysis. Thus, the
maximum number of replicates for any species within each treatment was 15, but
some were as low as 13 (when, for example, there were no survivors of a
particular species in each of two plots). The plant size index and number of
leaves, as well as amount of herbivory damage were averaged for all individuals
of each species in each plot, whereas survival was calculated as the fraction of
conspecifics within the same plot still alive after 190 days.
Two-way ANOVAs were used to assess the effects of plant species, the
treatment (slug-exposed and slug-excluded) and their interaction on the
responses listed above. The plant size index was log-transformed prior to
analysis in order to correct for disparities in variance among groups. Herbivore
damage was calculated as amount of leaf tissue removed (total from all leaves)
divided by the number of leaves on the plant (both whole and grazed). Within
each damage category only the high estimate (e.g. 25% in the 1-25% category)
was used, thus, herbivory damage estimates were not conservative. The
variance among groups was similar and residuals were normally distributed. All
statistical analyses were performed with Minitab® Release 14 (Ryan et al. 2005).
48
RESULTS
Plant growth
Final plant size (as measured using a size index) and number of leaves per plant
varied among species (Figures 3.2 and 3.3; for volume, F4,133 = 34.06, P < 0.001,
for number of leaves, F4,133 = 11.0, P < 0.001). But for both responses, neither
slug treatment nor slug treatment by plant species interaction contributed
significantly to total variation (for log transformed plant volume, F1,133 = 0.03, P =
0.859 for treatment and F4,133 = 0.21, P = 0.930 for treatment x species; for
number of leaves, F1,133 = 0.64, P = 0.426 for treatment and F4,133 = 0.83, P =
0.509 for treatment x species). Changes in plant volume and number of leaves
over time for each species and treatment are given in Appendix A and B
respectively.
Herbivory damage
Average damage per leaf at the end of the study period ranged from 10 to 30%
(Figure 3.4). There were no significant differences in final leaf damage between
the slug treatments (F1,133 = 0.36, P = 0.552), among plant species (F4,133 = 0.96,
P = 0.431), or as a result of a treatment by species interaction (F4,133 = 0.21, P =
0.933). Changes in leaf damage over time are given in Appendix C.
49
Seedling Survival
Within species effects
All plant species had increased mean survival in the slug-exclusion treatment,
but the magnitude of this increase was only significant for two of the five species
(Figure 3.5). Results of the ANOVA showed a significant effect due to the slug
treatment as well as a significant interaction between species and slug treatment
(Table 3.1), indicating that different plant species responded to slug herbivory to
differing degrees. When exposed to slugs, both endangered natives (C. superba
and S. obovata) experienced significantly higher mortality (Tukey’s HSD, P =
0.0065 and P = 0.0002, respectively). The majority of plant deaths occurred
within the first two months after planting (Figure 3.6).
Comparisons across species
While differences between the two tree species, N. sandwicensis and P.
cattleianum, were non-significant in the slug-excluded treatment (Tukey’s HSD, P
> 0 .05), in the slug-exposed treatment the native N. sandwicensis had
significantly lower survival than the alien P. cattleianum (Tukey’s HSD, P =
0.0315). A similar trend was observed for S. obovata, which when exposed to
slugs had significantly higher mortality than C. hirta (Tukey’s HSD, P = 0.0488)
and P. cattleianum (Tukey’s HSD, P < 0.0001), but under slug-excluded
conditions did not. In the slug-exposed treatment, C. superba differed
significantly only from P. cattleianum (Tukey’s HSD, P < 0.0001), and, again, this
50
difference in survival was eliminated when slugs were excluded (Tukey’s HSD, P
= 0.9505).
Seed bank regeneration
Very few seedlings emerged naturally within the plots during the six month
course of the study (Table 3.3). Clidemia hirta was most common, but it
averaged less than two seedlings per plot (four per m2). Although more seedlings
established in the slug-exposed plots than in the slug-excluded plots, this was
not statistically significant (Mann-Whitney, P = 0.88). For all other species, no
more than four seedlings total were found.
Slug monitoring
There was no significant difference in the number of slugs counted adjacent to
slug-exposed vs. slug-excluded plots (paired-T test, t = -1.19, P = 0.255).
Changes in total slug numbers (Figure 3.7) approximately tracked monthly
rainfall (National Weather Service Forecast Office 2004) with a correlation of r =
0.64, however this correlation was not statistically significant (P = 0.244).
DISCUSSION
In the Kahanahāiki Management Unit, slugs appear to be responsible for
substantial seedling mortality of certain native plant species. Of three native
species studied, two had significantly higher seedling mortality when exposed to
slugs. Both of these species (C. superba and S. obovata) are critically
51
endangered, and the 49-53% decrease in mean seedling survival as a result of
slug predation is probably an important factor underlying their current status. In
comparison, the seedlings of both introduced species (C. hirta and P.
cattleianum), which are highly abundant at the study site, were not significantly
impacted by slugs. The third native species tested, N. sandwicensis, also had
similar seedling survival in slug-excluded and slug-exposed plots. While this
species is not common at Kahanahāiki, adults make up a small proportion of the
canopy and subcanopy, and numerous seedlings were observed naturally
germinating underneath parent plants. The reasons that the latter three species
escape slug predation are unknown, but leaf toughness, which can influence slug
feeding (Dirzo 1980) may help protect both N. sandwicensis and P. cattleianum
while C. hirta grows rapidly enough to replace leaves lost to herbivory (S. Joe
pers. obs.). The chemical characteristics of these species, in addition to other
resistant species, should be investigated. Interestingly, none of the plant species
exhibited sub-lethal signs of slug herbivory: there were no significant differences
in plant size index, leaf number or herbivory damage scores among surviving
plants in the two treatments. Within the first two months, seedlings in the slugexposed treatment experienced high levels of mortality (Figure 3.6) suggesting
the plants were small enough that a single feeding event could result in death.
Additionally, this may indicate that slugs feed on most or all of a seedling before
moving on, killing the plant in a short amount of time.
52
Despite the small number of species tested, as well as their non-random
selection, my results suggest that slug herbivory may be skewing species
abundance in favor of non-native plants. In plots exposed to slug herbivory, the
rank order of mean seedling survival rates (with means in parentheses) was P.
cattleianum (90.7%), C. hirta (64.3%), N. sandwicensis (60.6%), C. superba
(37.3%) and S. obovata (35.6%). But when slugs were excluded, the rank order
changed to P. cattleianum (92.0%), C. superba (80.3%), C. hirta (77.3%), S.
obovata (70.0%) and N. sandwicensis (66.7%). Probably even more important
than the rank order is the fact that all native species survival rates were high, and
comparable to the introduced species. While other factors affect the rate at which
surviving seedlings will compete and persist to maturity, these results show that
slugs affect one important aspect of the process.
The low rate of natural seedling regeneration in both treatments points towards
additional factors impeding native seedling recruitment. These factors potentially
include reduced native seed rain (Moles and Drake 1999), low seed viability
(Baskin et al. 2004), lack of persistence in the seed bank (Drake 1998), the
destruction of seeds by predators (Garcia et al. 2005) and alteration of the soil
microclimate or chemical make-up (for example through allelopathy) (Macharia
and Peffley 1995). It is telling that the highly invasive C. hirta germinated the
most seedlings by far, and that its naturally germinated seedlings, like the
outplanted ones, were not impacted by slugs. A single individual can produce
over 500 fruits each season, each containing well over 100 seeds (Smith 1992);
53
this characteristic, combined with slug tolerance, helps explain its success at
Kahanahāiki and probably elsewhere.
Individual slug species appeared to respond to seasonal cues differently with M.
striatum appearing in May just as Deroceras sp. was disappearing. In contrast,
populations of D. reticulatum in temperate areas are known to peak between May
and June, after which they experience a decline until September (Hunter 1966),
when a second generation emerges, reaching its peak around October.
Based on the fact that the two native species negatively impacted by slugs in this
study are unrelated, it seems likely that other native species are also impacted by
slugs to some degree. As with other types of impact, the effects of slugs are
likely to be greatest on rare species. The implications are especially compelling
for rare plant restoration: outplanted seedlings that are unprotected from slug
predation may suffer significant mortality. Slugs now seem to occur in nearly all
mesic to wet habitat types in Hawai’i. A lack of slug distributional and abundance
data, however, makes it unclear whether slug densities at Kahanahāiki are
typical or anomalous, and therefore how representative these results are for
other natural areas. Additional studies should be conducted in other habitat
types, and with different focal plant species, to better understand the impact of
slugs in natural areas of Hawai‘i.
54
TABLES
Table 3.1. Seedling height (mm) by species on day 0 of the study.
Seedling
(Count)
Species
Mean
SEM
SD
Minimum
Maximum
90
Schiedea
obovata
43.1
2.28
21.73
10
100
150
Cyanea
superba
28.22
1.34
16.38
5
100
150
Clidemia
hirta
17.93
0.647
7.902
5
49
90
Nestegis
sandwicensis
40.53
1.9
18.08
10
84
150
Psidium
cattleianum
20.92
1.22
14.93
5
80
Table 3.2. Two-way ANOVA of seedling survival in slug-exposed and slugexcluded treatments.
Source of
variation
Adj MS
df
F-ratio
P
Treatment
1.43734
1
24.05
< 0.000
Plant species
0.66459
4
11.12
< 0.000
Treatment x plant
species
0.24883
4
4.16
< 0.003
Error
0.05975
140
Table 3.3. Number and identity of natural seedlings found in slug-exposed and
slug-excluded plots over 190 days.
Species
Count (Slugexposed)
Count (Slugexcluded)
Aleurites moluccana
2
0
Rubus rosifolius Sm.
4
0
R. rosifolius
0
3
Buddleia asiatica L.
0
1
Clidemia hirta
35
22
Pipturus albidus (Hook. & Arn.)
Gray
0
1
55
FIGURES
Figure 3.1. Location of Kahanahāiki Management Unit on the Island of O‘ahu.
56
Figure 3.2. Plant growth (using size index described in Materials and Methods) after 190 days in the slug-exposed vs.
slug-excluded treatment. No significant difference between treatments was found. Bars are ± one SEM.
57
Figure 3.3. Change in the number of leaves per plant after 190 days in the slug-exposed vs. slug-excluded treatment. No
significant difference between treatments was found. Bars are ± one SEM.
58
Figure 3.4. Average damage per leaf per plant in the slug-exposed vs. slug-excluded treatment grouped by plant species.
No significant difference between treatments or species was found. Bars are ± one SEM.
59
Figure 3.5. Survival by species after 190 days in the slug-exposed vs. slug-excluded treatment. Significantly higher
survival was observed for S. obovata and C. superba in the slug-excluded treatment (P < 0.05 *). Bars are ± one SEM.
60
Y axis = Survival (%)
X axis = Time elapsed from start of
experiment (days)
Figure 3.6. Seedling survival over time in slug-exposed vs. slug-excluded plots by species. Survival between monitoring
events is cumulative. Day 0 = 23 February 2004 and Day 190 = 1 September 2004. Bars are ± one SEM.
61
Figure 3.7. Counts of slugs frequenting cardboard traps April – August 2004 showing seasonal changes in the abundance
of different species and monthly rainfall.
62
APPENDIX A. Cumulative change in plant size index over time by species and slug herbivory treatment. Bars are ± one
SEM. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Slug Exposed vs. Slug Excluded treatments are
illustrated with dark vs. light grey shading.
63
Cumulative change in plant size index over time by species and slug herbivory treatment. Bars are ± one SEM. Day 0 =
February 22, 2004 and Day 190 = September 1, 2004. Slug Exposed vs. Slug Excluded treatments are illustrated with
dark vs. light grey shading.
64
Cumulative change in plant size index over time by species and slug herbivory treatment. Bars are ± one SEM. Day 0 =
February 22, 2004 and Day 190 = September 1, 2004. Slug Exposed vs. Slug Excluded treatments are illustrated with
dark vs. light grey shading.
65
Cumulative change in plant size index over time by species and slug herbivory treatment. Bars are ± one SEM. Day 0 =
February 22, 2004 and Day 190 = September 1, 2004. Slug Exposed vs. Slug Excluded treatments are illustrated with
dark vs. light grey shading.
66
Cumulative change in plant size index over time by species and slug herbivory treatment. Bars are ± one SEM. Day 0 =
February 22, 2004 and Day 190 = September 1, 2004. Slug Exposed vs. Slug Excluded treatments are illustrated with
dark vs. light grey shading.
67
APPENDIX B. Cumulative change in number of leaves per plant by species and slug herbivory treatment over time. Day 0
= February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug Excluded
treatments are illustrated with dark vs. light grey shading.
68
Cumulative change in number of leaves per plant by species and slug herbivory treatment over time. Day 0 = February
22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug Excluded treatments are
illustrated with dark vs. light grey shading.
69
Cumulative change in number of leaves per plant by species and slug herbivory treatment over time. Day 0 = February
22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug Excluded treatments are
illustrated with dark vs. light grey shading.
70
Cumulative change in number of leaves per plant by species and slug herbivory treatment over time. Day 0 = February
22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug Excluded treatments are
illustrated with dark vs. light grey shading.
71
Cumulative change in number of leaves per plant by species and slug herbivory treatment over time. Day 0 = February
22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug Excluded treatments are
illustrated with dark vs. light grey shading.
72
APPENDIX C. Change in damage per leaf by species and slug herbivory treatment over time. Gains and losses in leaf
surface area are cumulative. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug
Exposed vs. Slug Excluded treatments are illustrated with dark vs. light grey shading.
73
Change in damage per leaf by species and slug herbivory treatment over time. Gains and losses in leaf surface area are
cumulative. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug
Excluded treatments are illustrated with dark vs. light grey shading.
74
Change in damage per leaf by species and slug herbivory treatment over time. Gains and losses in leaf surface area are
cumulative. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug
Excluded treatments are illustrated with dark vs. light grey shading.
75
Change in damage per leaf by species and slug herbivory treatment over time. Gains and losses in leaf surface area are
cumulative. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug
Excluded treatments are illustrated with dark vs. light grey shading.
76
Change in damage per leaf by species and slug herbivory treatment over time. Gains and losses in leaf surface area are
cumulative. Day 0 = February 22, 2004 and Day 190 = September 1, 2004. Bars are ± one SEM. Slug Exposed vs. Slug
Excluded treatments are illustrated with dark vs. light grey shading.
77
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