THE EFFECTS OF A PARASITIC PLANT (CUSCUTA HOWELLIANA) ON VERNAL
POOL PLANT DIVERSITY
A Thesis
Presented to the faculty of the Department of Biological Sciences
California State University, Sacramento
Submitted in partial satisfaction of the requirements for the degree of
MASTER OF SCIENCE
in
Biological Sciences
(Ecology, Evolution and Conservation)
by
Andrea Graffis
FALL 2013
THE EFFECTS OF A PARASITIC PLANT (CUSCUTA HOWELLIANA) ON VERNAL
POOL PLANT DIVERSITY
A Thesis
by
Andrea Graffis
Approved by:
______, Committee Chair Jamie Kneitel, Ph.D.
______, Second Reader Patrick Foley, Ph.D.
______, Third Reader Shannon Datwyler, Ph.D.
______Date ii
Student: Andrea Graffis
I certify that this student has met the requirements for format contained in the University format manual, and that this thesis is suitable for shelving in the Library and credit is to be awarded for the thesis.
______, Graduate Coordinator ______Jamie Kneitel, Ph.D. Date
Department of Biological Sciences
iii
Abstract
of
THE EFFECTS OF A PARASITIC PLANT (CUSCUTA HOWELLIANA) ON VERNAL
POOL PLANT DIVERSITY
by
Andrea Graffis
Through the past 150 years over 90% of California’s vernal pool wetland habitat has been lost to agriculture and urbanization. Knowledge of the factors that drive species diversity in California’s vernal pools is required to enable proper management and restoration of these habitats in the future. While many factors have been identified as contributors to maintenance of species diversity in vernal pools, the system is far from being fully understood. One factor that has not been investigated is the effect of parasitic plants. Cuscuta howelliana is an abundant endemic parasitic plant that inhabits California vernal pools. The hypothesis tested in this research was that C. howelliana would act as a keystone predator and increase plant species diversity in vernal pools. This study took
place at Beale Air Force Base in the northeastern Sacramento Valley where there are
~1,000 vernal pools. In 15 vernal pools, experimental manipulation of the presence
versus absence of C. howelliana was conducted. An additional five vernal pools where C. howelliana was not naturally present were also monitored. Eryngium castrense and
Navarretia leucocephala were found to be the preferred host plant species of C. howelliana. Vernal pools without C. howelliana naturally present had lower plant species
iv
richness compared to pools where C. howelliana does occur naturally. Plots in vernal
pools where C. howelliana was manually removed also had lower plant species richness
compared to plots where C. howelliana was present. There was no single plant species
that showed a significant trend towards being absent in C. howelliana removal plots.
Eryngium castrense, one of the preferred host plants, had lower percent cover in plots where C. howelliana was present, which may have explained differences in species richness. However, most plant species on average showed a higher percent cover in C. howelliana present plots, but this did not become significant until all plant species were considered on one model. Grazing regime differences among vernal pools with C. howelliana naturally present and naturally absent may have also contributed to the
observed difference in plant species richness. In conclusion, C. howelliana presence was
related to increases in species richness, consistent with what is expected from the effects
of a keystone predator. Interactions among species, including parasitic plants, needs to be
considered in restoration and management of California vernal pools.
______, Committee Chair Jamie Kneitel, Ph.D.
______Date
v
ACKNOWLEDGEMENTS
Thanks to the staff at Beale Air Force Base for allowing me the use of their
facilities, the California Native Plant Society for providing funding, Jamie Kneitel,
Patrick Foley, Shannon Datwyler and James Baxter for providing guidance and Alison
Wagner for providing field assistance.
vi
TABLE OF CONTENTS
Page Acknowledgements ...... vi
List of Tables ...... viii
List of Figures ...... x
Introduction ...... 1
METHODS ...... 7
Study Site ...... 7
Vernal Pool Zones...... 7
Host Plant Preference ...... 10
C. howelliana’s Effect on Plant Diversity ...... 13
RESULTS ...... 16
Density and Host Preference ...... 16
C. howelliana’s Effect on Plant Diversity ...... 24
DISCUSSION ...... 42
Host Preference ...... 42
C. howelliana Removal Plots ...... 45
Vernal Pools without C. howelliana Present ...... 48
Other Parasitic Plants and Management Implications ...... 49
CONCLUSION ...... 51
Literature Cited ...... 52
vii
LIST OF TABLES
Tables Page
Table 1. Prevalence of plant species parasitized by C. howelliana in
2012 (n = 16)...... 18
Table 2. Characteristics of plant species that were not parasitized by C.
howelliana in 2012 (n = 16)...... 20
Table 3. Within-Subject effects of repeated measures general linear model
for a dependent variable of plant species richness...... 27
Table 4. Within-Subject effects of repeated measures general linear model
for a dependent variable of total plant percent cover...... 29
Table 5. All plant species (n = 29) found during the 2013 sampling and
the type of vernal pool inhabited by each species...... 30
Table 6. Tests of fixed effects from the linear multilevel mixed model
with plant species richness as the dependent variable...... 33
Table 7. Tests of fixed effects from the linear multilevel mixed model
with total plant cover as the dependent variable...... 34
Table 8. Within-Subject effects of repeated measures general linear model
for a dependent variable of E. castrense percent cover...... 36
Table 9. Tests of fixed effects from the linear multilevel mixed model
with E. castrense percent cover as the dependent variable...... 38
viii
LIST OF TABLES
Tables Page
Table 10. Within-Subject effects of repeated measures general linear
model for a dependent variable of N. leucocephala percent
cover...... 39
Table 11. Tests of fixed effects from the linear multilevel mixed model
with N. leucocephala percent cover as the dependent variable...... 41
ix
LIST OF FIGURES
Figures Page
Figure 1. Vernal pool depicting edge, transition, and center zones ...... 9
Figure 2. Map of study site at Beale Air Force Base ...... 12
Figure 3. Percent cover of C. howelliana by location with the vernal pools ...... 17
Figure 4. E. castrense covered by C. howelliana when E. castrense cover
is normalized for total plant cover ...... 22
Figure 5. N. leucocephala covered by C. howelliana when N.
leucocephala cover is normalized for total plant cover ...... 23
Figure 6.Effect of the presence or absence of C. howelliana and C.
howelliana removal in a vernal pool on plant species richness ...... 28
Figure 7. Effect of the presence or absence of C. howelliana and C.
howelliana removal in a vernal pool on total plant percent cover ...... 35
Figure 8. Effect of the presence or absence of C. howelliana in a vernal
pool on E. castrense percent cover ...... 37
Figure 9. Effect of the presence or absence of C. howelliana and C.
howelliana removal in a vernal pool on N. leucocephala percent
cover ...... 40
x
1
INTRODUCTION
Wetlands worldwide are subject to degradation of species diversity and ecosystem
function because of human activities (Mitsch & Gosselink 2007). Therefore, it is essential
to understand the ecological mechanisms that affect and maintain species diversity in
these communities. Historically, ecologists have focused on competitive interactions, but over the past several decades the role of predators and parasites in communities have gained increasing attention (Paine 1966, Janzen 1970, Connell 1971).
The theory of keystone predation makes the prediction that a predator, which consumes a competitively dominant prey, will increase species diversity in an ecosystem
(Paine 1966). Similarly, the Janzen-Connell hypothesis discussed how specialist enemies such as predators, parasites, or herbivores can have density-dependent effects that optimize species richness and minimizes the opportunity for monoculture formation
(Janzen 1970, Connell 1971). These effects have been documented in various predators
(Paine 1966, Ester & Palmisano 1974), herbivores (Bowers et al. 1987, Naiman et al.
1986), and parasites (Grewell 2008, Pennings 1996, Watson 2009). However, parasitic plants have been relatively less studied.
Thousands of parasitic plant species are found worldwide (Kuijt 1969). Studies have found that parasitic plants can have either positive or negative effects on species diversity in communities (Pennings & Callaway 2006, Press & Phoenix 2005). For example, Rhinanthus minor, a hemiparasitic plant, has been found to decrease diversity of sand dune communities by preferentially parasitizing a competitively inferior species
2
(Gibson & Watkinson 1989, Press & Phoenix 2005). In contrast, Amyema miquelii, a mistletoe, increased plant species diversity in eucalyptus forests of south-eastern
Australia by two pathways. First, A. miquelii increased leaf litter accumulation, which created more habitat and nutrient availability for decomposers and other plants. Second,
A. miquelii also provided a continuous source of flowers for pollinators and fruits for herbivores and seed dispersers (Watson 2009). The parasitic plant Cuscuta salina has also been shown to increase plant diversity in coastal wetlands where their preferred host plant, Salicornia virginica, is competitively dominant (Grewell 2008, Pennings 1996).
Cuscuta salina created open habitat patches for competitively inferior plants by suppression of the dominant plant species. It is still unclear if the majority of parasitic plants can structure their surrounding communities in this way.
Although Cuscuta species are considered generalists in host compatibility, studies have found evidence of host preferences in this genus. For example, Cuscuta europaea were presented with a host, Crataegus monogyna, which had varying nutrient availability in their tissues (Kelly 1992). Cuscuta europaea rejected C. monogyna as a host when it had low nutrient availability in its tissues. In another study by Koch et al. (2004), Cuscuta campestris selectively foraged for the most suitable host in a heterogeneous plant community. These behaviors by plants in the genus Cuscuta may lead to significant effects on the composition of the surrounding plant community, especially when the host is a dominant species in the community.
3
Cuscuta howelliana, or Boggs Lake Dodder, is an endemic species of Cuscuta
that inhabits vernal pools throughout California (Costea & Stefanović 2012). Cuscuta
howelliana is an obligate annual vine parasite. It does not have the ability to
photosynthesize. This trait is apparent in the plants orange color and vestigial leaves. The plant mines its nutrients through its haustoria that tap into the host plants phloem (Kuijt
1969). The genus Cuscuta is in the otherwise non-parasitic family Convolvulaceae
(Baldwin et al. 2012). The C. howelliana treatment in the Jepson Manual states that C. howelliana lives on vernal pool margins and generally parasitizes Eryngium, Navarretia,
Polygonum polygloides subspecies kelloggi, and Epibolium campestre (Costea &
Stefanović 2012). Despite research showing that parasitic plants can have a large effect on community composition, little is known about the effects C. howelliana has on plant community composition in vernal pools.
California vernal pools, the habitat that C. howelliana is endemic to, support a diverse community of over 70 endemic plant and invertebrate species (Baldwin et al.
2012, Stone 1990). Recent replacement of 90%-97% of vernal pool habitat with agriculture and urbanization has coincided with many endemic vernal pool species becoming endangered (Holland & Jain 1988, Holland 1998). For these reasons,
California vernal pools are the focus of much ecological research on management and mitigation of endangered and threatened species (US Fish & Wildlife Service 2005,
Witham 2006).
4
Vernal pools are ephemeral wetlands that occur in shallow depressions with
impermeable hardpans beneath the soils. The annual cycle of a vernal pool is
characterized by inundation during the winter rainy season, a gradual evaporation of the water in the spring, and complete desiccation in the summer and early fall. Most vernal pools in California are found in the grasslands of the central valley and the western foothills of the Sierra Nevada. However, vernal pools also occur in coniferous forests, chaparral, coastal scrub, and oak woodlands (Holland & Jain 1981). The diverse plants that live in vernal pools are uniquely adapted to long alternating periods of inundation and desiccation (Spencer & Rieseberg 1998). Examples of these adaptations include an annual life cycle to tolerate the extremes in water availability and germination during
inundation followed by rapid growth once desiccation of the pool begins (Holland & Jain
1988).
Many mechanisms for maintenance of diversity have been identified in vernal
pools. For example, the annual cycle of inundation with rain water and desiccation in the
dry season creates a heterogeneous environment with different inundation durations at
different pool depths. This heterogeneity in abiotic conditions maintains diversity by
harboring endemic plants with differing tolerances to inundation gradients (Emery 2009,
Bauder 2000) and excludes non-native species that lack tolerance to these environmental
extremes (Gerhardt and Collinge 2003). Other factors such as the presence of specialist
pollinators (Thorp 1998), properly controlled agricultural grazing (Marty 2004, Croel and
Kneitel 2011), depth and surface area of a pool (King et al. 1996), and island
5 biogeography (Holland and Jain 1981) have all shown to be contributors to diversity and species coexistence in vernal pools.
While many factors have been identified as contributors to diversity in vernal pools, the system is far from being fully understood. One factor that has not been investigated is the effect of parasitic plants. Little is known about the community effects of the parasitic plant C. howelliana, which commonly inhabits California vernal pools
(Baldwin et al. 2012). Knowledge of factors that maintain vernal pool diversity is also particularly useful in the implementation of restoration and mitigation projects for vernal pool habitat.
If there is a decrease in abundance of a competitive dominant plant due to parasitism by C. howelliana, this may create opportunities for less competitive plants to grow. Consequently, C. howelliana may act as a keystone predator in vernal pools. This possible interaction would lead to a cause for including C. howelliana in vernal pool restoration and management efforts in order to help maintain plant species richness.
Investigating the effect of C. howelliana on vernal pool plant diversity would also contribute to a more complete understanding of the role parasitic plants play in shaping community composition.
The objective of this study was to understand the role of C. howelliana in
California vernal pools. To this end, how C. howelliana infection varies within and across vernal pools and their host preferences were determined. The hypothesis was that C. howelliana increases plant species diversity in vernal pools and a removal experiment
6 was conducted to assess the cover and richness response of the vernal pool plant community to the presence and absence of C. howelliana.
7
METHODS
Study Site
This study took place at Beale Air Force Base in Yuba County, California. Beale
Air Force Base is located in northeastern Sacramento Valley at the foot of the Sierra
Nevada mountain range. There are about 1,000 vernal pools within Beale Air Force Base.
The elevation of Beale Air Force Base ranges from 24-180m. Most of the about 8,000 ha of undeveloped land at Beale Air Force Base is vernal pool grassland habitat (Platenkamp
1998) and is regularly grazed by cattle, including the study site. The geological formation underlying the vernal pools sampled from is Riverbank and Modesto formation. Both formations originated in the Pleistocene and are composed of a relatively small amount of granitic sand stratified on top of a dark red clay and silt. The vernal pools sampled from are in a 2.5 km2 area well known to contain C. howelliana.
Vernal Pool Zones
There are three easily distinguishable zones within a vernal pool: center zone,
transition zone, and edge zone (Emery et al. 2009). The center zone refers to the deepest
part of a vernal pool that is inundated for the longest period of time. The center zone
usually contains only native plants adapted for inhabiting long periods of inundation and
saturated soil conditions. The transition zone refers to the portion of a vernal pool that
circles the center zone. The transition zone dries out before the center zone, but is still
inundated for a long enough time period to exclude most non-vernal pool plant species.
8
The edge zone refers to the area of a vernal pool that dries out quickly after a pool reaches maximum water capacity. Plants that inhabit the edge of a vernal pool are a mixture of vernal pool and upland grassland plants (Figure 1).
9
Center
Transition
Edge
Figure 1. Vernal pool depicting edge, transition, and center zones.
10
Host Plant Preference
In late May and early June of 2012, C. howelliana infection level within the three vernal pool zones and the C. howelliana host plant preferences were investigated. Fifteen vernal pools were chosen randomly during the peak of the C. howelliana growing season
(Figure 2). The 15 vernal pools were chosen from a 2.5km2 area of land at that Beale Air
Force Base staff approved for use. A 0.25m2 quadrat was used for randomly sampling
twice in the center, transition, and edge zones of each of the 15 vernal pools.
Vernal pool plants tend to distribute themselves according to the inundation
gradient as previously described as the three zones (center, transition, and edge) of a
vernal pool (Gerhardt & Collinge 2003, Emery et al. 2009). Therefore, it is possible that
C. howelliana would vary in its distribution in relation to this gradient as well. To
determine a possible C. howelliana vernal pool zone preference, percent C. howelliana
cover data was used from each of the sampling locations of each vernal pool. An
ANOVA was conducted on this data. To test for difference among groups, a post hoc test
with a Bonferroni correction was conducted.
Cuscuta howelliana host preference was determined by quantifying the number
of plants from each species that were parasitized in each sampling location and what
percent of the total C. howelliana present in each plot occurred on each host plant
species. A large number of Eryngium castrense and Navarretia leucocephala individuals compared to other plant species were parasitized by C. howelliana. To investigate
whether the use of those host species was frequency dependent, the percent E. castrense
11 or N. leucocephala cover relative to the total plant cover was compared to the percent of
E. castrense or N. leucocephala covered by C. howelliana. A regression analysis was then done to determine any relationship between these variables.
12
Figure 2. Map of study site at Beale Air Force Base. Red shapes encompass the vernal pools sampled from (n=20).
13
C. howelliana’s Effect on Plant Diversity
To test the hypothesis that C. howelliana will increase plant species diversity in
vernal pools, experimental manipulation of C. howelliana presence and absence was
conducted. A set of paired 0.25 m2 plots were placed in the center and at the transition
zones in each of the 15 vernal pools when C. howelliana began to germinate on March
24, 2013 (Figure 2). In one of each paired plots, germinating C. howelliana was removed
manually. Seedlings were removed once a week until there were no longer seedlings
emerging. Seedlings of C. howelliana were easily distinguished from other plants due to
their lack of cotyledons and orange color. If seedlings were able to reach a host plant and
make any haustoria connections, they were severed to allow the host plant to develop
normally (Pennings & Callaway 2002). Germinating C. howelliana individuals in the
other of each paired plot were allowed to grow.
From the preliminary research conducted (see below) it was found that C. howelliana does not inhabit the edges of vernal pools, so edges were not used in the manipulative portion of this study. Each plot pair was placed 0.5 m apart at the same elevation within a pool to obtain the best approximation of equal abundance and richness of plant species initially. For comparison, five pools where C. howelliana was not naturally present were sampled as well (Figure 2). Within these five pools, two 0.25m2
plots were placed in both the center and transition zones.
Plant species richness (using Baldwin et al. 2012) and percent cover were measured in each 0.25 m2 plot every two weeks. By placing a 100 cell grid over each of
14
the 0.25 m2 paired plots, percent cover was the number of grid squares covered by any
one species (Meese & Tomich 1992). Sampling ceased once C. howelliana completed
flowering. The first sampling period was not conducted in the five vernal pools where C.
howelliana is not naturally present because of a large number of aggressive bulls. This is
accounted for in all analysis conducted.
The data from the 15 vernal pools where the C. howelliana removal experiment
was conducted were analyzed through repeated measures general linear models using
SPSS version 21 (IBM Corp. 2012). The goal was to determine if the treatment received
by a plot was a predictor of any of the dependent variables. The dependent variables
tested included: total percent cover of all non-Cuscuta plants, total plant species richness,
and each plant species percent cover within all plots sampled.
Also using SPSS version 21, linear multilevel mixed effect models were used to
determine if the presence of C. howelliana in a vernal pool was a predictor of any of the
dependent variables (IBM Corp. 2012). The repeated measures general linear model was not used here due to unbalanced sampling design. The data used for this analysis included
the C. howelliana removal plots from the 15 vernal pools with C. howelliana naturally
present, but exclude the data from C. howelliana present plots from the vernal pools with
C. howelliana naturally present. Sampling period and vernal pool type (C. howelliana
naturally present and C. howelliana naturally absent) were fixed effects. Individual vernal
pools and locations within pools were used as random effects. The plots were sampled
15 every two weeks resulting in five sampling periods. Therefore, sampling period was used as a repeated measure.
16
RESULTS
Density and Host preference
Within the 15 vernal pools sampled, C. howelliana obtained a mean percent cover of 5.07% ± standard deviation of 3.19% and ranged from 0.4% to 11%. Cuscuta howelliana density was significantly different among pool locations
(F = 7.791, df = 44, P = 0.001; Figure 3). Cuscuta howelliana percent cover was highest in the center and transition zones and was only rarely present in the edge zone. Of the
1,365 parasitized plants, E. castrense and N. leucocephala together make up 1,151, or
84.3%, of all the individual plants parasitized by C. howelliana. Eryngium castrense comprised 61.35% of the C. howelliana cover. N. leucocephala comprised 28.6% of the
C. howelliana cover (Table 1). Of the 32 plant species observed, only half (16) of them were parasitized by C. howelliana (Table 1, Table 2). Cuscuta howelliana parasitism was associated with vernal pool endemics (versus wetland generalists or non-native species)
(Pearsons Χ2= 4.8, P = 0.028).
The relationship between percent E. castrense covered by C. howelliana and the
percent E. castrense cover (normalized by total plant cover) was a negative exponential
function (r2 = 0.409, P = 0.001, y = -10.273Ln(x) + 64.124; Figure 4). There was no
relationship found with N. leucocephala (r2 = 0.117, P = 0.230; Figure 5).
17
12 B 10
8 B 6 Percent Cover (%) 4
2 A
0
C. howelliana Edge Transition Center Vernal Pool Zone
Figure 3. Percent cover of C. howelliana by location with the vernal pools. Error bars represent standard error. From ANOVA, F = 7.791, df = 44, P = 0.001. The letters indicate differences based on post hoc test with Bonferroni correction.
18
Table 1. Prevalence of plant species parasitized by C. howelliana in 2012 (n = 16).
Parasitized Plants Percent of Native Number of Total C. Species (Family) Status for Habitat Plants howelliana California Parasitized Cover
Isoetes orcuttii Native Vernal Pools 0.08 1 (Isoeteaceae)
Eleocharis Native Wetlands 1.12 32 macrostachya (Cyperaceae)
Aira caryophyllea Exotic Grasslands 0.23 1 (Poaceae)
Polypogon Exotic Wetlands 1.59 22 monspeliensis (Poaceae)
Eryngium castrense Native Vernal Pools 61.35 155 (Apiaceae)
Hemizonia fitchii Native Wetlands 0.52 8 (Asteraceae)
Psilocarphus Native Vernal Pools 0.08 2 brevissimus (Asteraceae)
Leontodon taraxacoides Exotic Wetlands 0.73 19 (Asteraceae)
Lasthenia glaberrima Native Vernal Pools 0.65 7 (Asteraceae)
19
Table 1 Continued.
Parasitized Plants Percent of Number of Native Status Total C. Species (Family) Habitat Plants for California howelliana Parasitized Cover
Lasthenia Native Vernal Pools 1.87 31 fremontii (Asteraceae)
Plagiobothrys Native Vernal Pools 0.79 39 stipitatus (Boraginaceae)
Downingia Native Vernal Pools 2.02 24 bicornuta (Campanulaceae)
Lythrum Exotic Wetlands 0.47 8 hyssopifolia (Lythraceae)
Castilleja Native Wetlands 0.84 18 campestris (Orobanchaceae)
Navarretia Native Vernal Pools 28.60 996 leucocephala (Polemoniaceae)
Ranunculus Native Vernal Pools 0.35 2 aquatilis (Ranunculaceae)
20
Table 2. Characteristics of plants species that were not parasitized by C. howelliana in
2012 (n = 16).
Non-Parasitized Plants Native Status for Species (Family) Habitat California
Alopecurus saccatus Native Vernal Pools (Poaceae)
Agrostis avenacea Exotic Grasslands (Poaceae)
Briza minor Exotic Grasslands (Poaceae)
Lolium multiflorum Exotic Grasslands (Poaceae)
Taeniatherum caput- Exotic Grasslands medusae (Poaceae)
Fescuta bromoides Exotic Grasslands (Poaceae)
Juncus bufonius Native Wetlands (Juncaceae)
Brodiaea minor Native Wetlands/Grasslands (Themidaceae)
Layia fremontii Native Wetlands/Grasslands (Asteraceae)
21
Table 2 Continued.
Non-Parasitized Plants Species (Family) Native Status for California Habitat
Cuscuta Native Vernal Pools howelliana (Convolvulaceae)
Elatine rubella Native Wetlands (Elatinaceae)
Croton setiger Native Grasslands (Euphorbiaceae)
Trifolium dubium Exotic Grasslands (Fabaceae)
Erodium botrys Exotic Grasslands (Geraniaceae)
Mimulus tricolor Native Vernal Pools (Phrymaceae)
22
90 80 70 60 50
E. castrense 40 30 20
Percent 10 Cover/Total Plant Cover Plant Cover/Total 0 0 50 100 150 200 250 300 Percent E. castrense covered by C. howelliana
Figure 4. E. castrense covered by C. howelliana when E. castrense cover is normalized for total plant cover (r2 = 0.409, P = 0.001, and y = -10.273ln(x) + 64.124).
23
90 80 70 60 50 40
N. leucocephala N. leucocephala 30 20 10 Cover/Total Plant Cover Plant Cover/Total Percent 0 0 10 20 30 40 50 Percent N. leucocephala Covered by C. howelliana
Figure 5. N. leucocephala covered by C. howelliana when N. leucocephala cover is normalized for total plant cover (r2 = 0.117, P = 0.230).
24
C. howelliana’s Effect on Plant Diversity
Plant species richness in vernal pools with C. howelliana was strongly influenced
by the treatment received in the plot (F = 35.710, df = 1, P < 0.001; Table 3). In plots
with C. howelliana intact, plant species richness was greater, ranging from 10% higher in
late March to 30% higher in late May, compared to plots with C. howelliana removed
(Figure 6). Total plant cover between C. howelliana removal plots and C. howelliana
presence plots did not differ significantly (F = 2.962, df = 1, P= 0.125; Table 4).
In C. howelliana naturally present vernal pools there were 29 total plant species
found within all plots. In C. howelliana naturally absent vernal pools there were only 23
total plant species found within all the plots. There were no plant species found within C.
howelliana naturally absent vernal pool and not within C. howelliana naturally present
vernal pools (Table 5). All plant species in C. howelliana absent vernal pools were
present C. howelliana present vernal pools. Plant species richness in a vernal pool was
significantly greater in the presence of naturally occurring C. howelliana compared to
vernal pools with C. howelliana naturally absent (F = 13.607, df = 1, P = 0.001; Table 6).
In vernal pools with C. howelliana naturally present, plant species richness ranged from
18% higher in late March to 105% higher in late May compared to vernal pools with C. howelliana naturally absent (Figure 6; Table 6). Total plant cover was significantly greater in the presence of naturally occurring C. howelliana in the vernal pool
(F = 57.217, df = 1, P < 0.000; Table 7). In vernal pools with C. howelliana naturally absent, total plant species cover ranged from 36% lower in early March to 60% lower in
25
late May compared to vernal pools with C. howelliana naturally present
(Figure 7; Table 7).
Eryngium castrense, one of the preferred hosts, had significantly higher cover in
C. howelliana removal plots (F = 7.597, df = 1, P = 0.015; Table 8). From early March to the end of April, the E. castrense percent cover was not different between the treatments.
Beginning in late April, the E. castrense percent cover began to decrease in the C.
howelliana presence plots and increase in the C. howelliana absent plots. At the end of
May, E. castrense cover was 43% higher in the C. howelliana absent plots compared to
the C. howelliana present plots (Figure 8). Eryngium castrense percent cover was significantly greater in vernal pools with naturally occurring C. howelliana
(F = 10.005, df = 1, P = 0.005; Table 9). In vernal pools with C. howelliana naturally absent, E. castrense percent cover ranged from 60% lower in late March to 70% lower in late May compared to C. howelliana removal plots (Figure 8; Table 9).
Navarretia leucocephala, another of the preferred hosts of C. howelliana, percent cover was not influenced by the removal treatment (F = 1.703, df = 1, P = 0.210; Table
10). In both experimental plots, N. leucocephala percent cover ranged from 0–50% during the first five sampling periods. During the last sampling period, the majority of the
N. leucocephala had finished its life cycle (Figure 9). In vernal pools with C. howelliana absent, N. leucocephala percent cover also did not differ compared to C. howelliana removal plots (F = 1.356, df = 1, P = .261; Figure 9; Table 11). All other plant species
26 observed did not have significant cover differences between C. howelliana removal plots and C. howelliana presence plots.
27
Table 3. Within-Subject effects of repeated measures general linear model for a dependent variable of plant species richness.
Type III Mean Source Sum of df F p-value Square Squares
Time 1035.17 5 207.034 79.065 < 0.001
Location 13.360 1 13.360 3.235 0.095
Treatment 87.027 1 87.027 35.710 <0.001
Time * 9.622 5 1.924 1.470 0.212 Location
Time * 10.741 5 2.148 2.395 0.047 Treatment
Location * 0.503 1 0.503 0.128 0.727 Treatment Time * Location * 4.265 5 0.853 1.051 0.396 Treatment
28
12
10 C. howelliana 8 Present Plots
6 C. howelliana Removal Plots Richness (S) 4 C. howelliana 2 Absent Pools
0 7-Apr 5-May 14-Apr 21-Apr 28-Apr 24-Mar 31-Mar 12-May 19-May 26-May Time Figure 6. Effect of the presence or absence of C. howelliana and C. howelliana removal in a vernal pool on plant species richness. Error bars represent standard error.
29
Table 4. Within-Subject effects of repeated measures general linear model for a dependent variable of total plant percent cover.
Type III Mean Source Sum of df F p-value Square Squares
Time 30486.821 5 6097.364 42.787 < 0.001
Location 1265.190 1 1265.190 1.811 0.201
Treatment 462.012 1 462.012 2.692 0.125
Time * 5 1.900 Location 1826.452 365.290 0.106
Time * 5 Treatment 1749.417 349.883 3.828 0.004
Location * 1 Treatment 68.762 68.762 0.326 0.578 Time * Location * 203.667 5 40.733 0.592 0.706 Treatment
30
Table 5. All plant species (n = 29) found during the 2013 sampling and the type of vernal pool inhabited by each species. Present = C. howelliana naturally present vernal pools,
Both = C. howelliana naturally present and naturally absent vernal pools.
Species (Family) Vernal Pool Type Inhabited
Eleocharis marcostachya Both (Cyperaceae)
Juncus uncialis Both (Junceae)
Juncus capitatus Both (Juncaceae)
Polypogon monsplensis Both (Poaceae)
Aira caryophyllea Both (Poaceae)
Lolium multiflorum Both (Poaceae)
Taeniatherum caput- medusae Both (Poaceae)
Brodiaea elegans Both (Themidaceae)
Both Eryngium castrense (Apiaceae)
Both Lasthenia fremontii (Asteraceae)
31
Table 5 Continued.
Species (Family) C. howelliana Present Pools
Lasthenia glabberima Present (Asteraceae)
Hemizonia fitchii Both (Asteraceae)
Psilocarphus Both brevissimus (Asteraceae)
Leontodon taraxacoides Both (Asteracese)
Plagiobothrys stipitatus Both (Boraginaceae)
Downingia cuspidate Present (Campanulaceae)
Downingia bicornuta Both (Campanulaceae)
Crassula aquatica Both (Crassulaceae)
Croton setiger Both (Euphorbiaceae)
Cicendia quadrangularis Both (Gentianaceae)
Mentha pulegium Both (Lamiaceae)
Pogogyne douglasii Present (Lamiaceae)
32
Table 5 Continued.
Species (Family) C. howelliana Present Pools
Linum bienne Both (Lamiaceae)
Lythrum hyssopifolium Both (Lythraceae)
Gratiola ebracteata Both (Plantaginaceae)
Plantago lanceolata Present (Plantaginaceae)
Navarretia leucocephala Both (Polemoniaceae)
Castilleja campestris Both (Orobanchaceae)
Ranunculus bonariensis Present (Ranunculaceae)
33
Table 6. Tests of fixed effects from the linear multilevel mixed model with plant species richness as the dependent variable.
Numerator Denominator Source F p-value df df
Pool Type 1 13.607 16.214 0.001
Time 4 134.522 52.914 < 0.001
34
Table 7. Tests of fixed effects from linear multilevel mixed model with total plant percent cover as the dependent variable.
Numerator Denominator Source F p-value df df
Pool Type 1 34.133 57.217 < .001
Time 4 173.320 26.806 < .001
35
80 70 60 C. howelliana Present Plots 50 40 C. howelliana Removal Plots 30 C. howelliana Total Plant Cover (%) 20 Absent Pools 10 0 7-Apr 5-May 14-Apr 21-Apr 28-Apr 24-Mar 31-Mar 12-May 19-May 26-May Time
Figure 7. Effect of the presence or absence of C. howelliana and C. howelliana removal in a vernal pool on total plant percent cover. Error bars represent standard error.
36
Table 8. Within-Subject effects of repeated measures general linear model for a dependent variable of E. castrense percent cover.
Type III Mean Source Sum of df F p-value Square Squares
Time 972.514 5 194.503 0.587 0.710
Location 420.336 1 420.336 2.016 0.178
Treatment 1120.069 1 1120.069 7.597 0.015
Time * 5 0.363 Location 153.781 30.756 0.872
Time * 5 Treatment 1883.381 376.676 25.118 < 0.001
Location * 1 Treatment 9.669 9.669 0.057 0.814 Time * Location * 99.047 5 19.809 1.313 0.269 Treatment
37
35
30
25 C. howelliana Present Plots 20 Cover (%) C. howelliana 15 Removal Plots
10 C. howelliana E. castrense Absent Pools 5
0 7-Apr 5-May 14-Apr 21-Apr 28-Apr 24-Mar 31-Mar 12-May 19-May 26-May Time
Figure 8. Effect of the presence or absence of C. howelliana and C. howelliana removal in a vernal pool on E. castrense percent cover. Error bars represent standard error.
38
Table 9. Tests of fixed effects from linear multilevel mixed model with E. castrense percent cover as the dependent variable
Numerator Denominator Source F p-value df df
Pool Type 1 17.766 10.005 0.005
Time 4 165.122 6.406 < 0.001
39
Table 10. Within-Subject effects of repeated measures general linear model for a dependent variable of N. leucocephala percent cover.
Type III Sum of Source df Mean Square F p-value Squares
Time 4020.581 5 814.116 1.760 0.133
Location 1 407.469 407.469 1.725 0.210
Treatment 123.669 1 123.669 1.703 0.213
Time* 5 0.569 Location 400.981 80.196 0.724
Time* 5 Treatment 50.314 10.063 0.976 0.438
Location* 1 Treatment 0.469 0.469 0.095 0.762 Time* Location* 62.114 5 12.423 2.642 0.030 Treatment
40
18 16 14 C. howelliana 12 Present Plots 10 C. howelliana 8 Removal Plots
6 C. howelliana 4 Absent Pools N. Cover (%) leucocephala 2 0 7-Apr 5-May 14-Apr 21-Apr 28-Apr 24-Mar 31-Mar 12-May 19-May 26-May Time
Figure 9. Effect of the presence or absence of C. howelliana and C. howelliana removal in a vernal pool on N. leucocephala percent cover. Error bars represent standard error.
41
Table 11. Tests of fixed effects from linear multilevel mixed model with N. leucocephala percent cover as the dependent variable.
Numerator Denominator Source F p-value df df
Pool Type 1 16.141 1.356 0.261
Time 4 150.813 15.453 < .001
42
DISCUSSION
The objective of this study was to determine the role of Cuscuta howelliana in the
vernal pool plant community. Cuscuta howelliana occurs in the deeper areas of vernal
pools, and does not occur around the edge of vernal pools. Eryngium castrense and
Navarretia leucocephala were found to be the preferred hosts for C. howelliana.
Experimental removal of C. howelliana found E. castrense percent cover in a vernal pool
was negatively affected by C. howelliana presence, but N. leucocephala percent cover
was not affected. When C. howelliana was naturally absent in a vernal pool or removed
from a small area of a vernal pool, plant species richness decreased. Lastly, this research
found that total plant cover in a vernal pool decreases when C. howelliana is not naturally
present.
Host Preference
Although there were 16 total plant species with clear haustoria connections,
E. castrense and N. leucocephala were the preferred hosts of C. howelliana. The negative
relationship between percent E. castrense covered by C. howelliana and the standardized
percent E. castrense, suggested early in the research that C. howelliana may negatively affect the percent cover that E. castrense can reach in vernal pools (Figure 4). This same relationship did not exist with N. leucocephala, which implies that C. howelliana may not have the same affect on N. leucocephala cover in vernal pools. This analysis shows that
C. howelliana potentially reduces the percent cover that E. castrense is able to achieve
43
and has no effect on the percent cover N. leucocephala is able to achieve. This might mean that C. howelliana may be drawing more resources from E. castrense than from N. leucocephala. If this is the correct reason for the correlation shown in the analysis of E. castrense, it shows a higher preference of C. howelliana for E. castrense over N. leucocephala. Numerous studies have shown that parasitism reduces host productivity
(Howell and Mathiasen 2004, Silva 1996, Tennakoon and Pate 1996). Therefore, if C. howelliana prefers E. castrense to N. leucocephala, it will draw more resources from that host.
The two preferred host plant species only rarely occur on the edge zones of a vernal pool. This may, in part, explain why C. howelliana is only rarely observed in the edge zone as well (Figure 3). However, the restriction of C. howelliana to the deeper portions of a vernal pool could be due to other factors such as hosts access to limiting nutrients (Pate et al. 1990) or C. howelliana preference for less stressed hosts (Miller et al. 2003).
Plants of non-preferred host species that were being parasitized appeared to have fewer haustoria connections (Graffis, personal observation). Fewer haustoria connections might imply that the C. howelliana plant is drawing fewer resources from the less preferred but parasitized host plants. This trend was also seen in Cuscuta subinclusa, which coils more around a more preferred host plant and in turn create more haustoria connections (Kelly 1990). A similar pattern was also observed with Cuscuta europaea, which only parasitized hosts with higher nutrient availability (Kelly 1992).
44
Of the 32 observed plant species in the sample plots, 16 species were not
parasitized at all. Cuscuta howelliana did make contact and wrapped around these non-
parasitized species, but did not make haustoria connections. This wrapping might
function as a structure for the C. howelliana to use for growing towards a desired host
plant. Species in the genus Cuscuta have shown the ability to selectively forage in a
heterogeneous plant community, which helps support this explanation (Koch et al. 2004,
Gibson and Watkinson 1989).
The C. howelliana individuals only produced flowers within the inflorescences of
E. castrense and N. leucocephala, the two preferred host plant species. During 2012, C. howelliana produced flowers within the inflorescences of both E. castrense and N. leucocephala. However, during 2013 C. howelliana flowers were observed only within the inflorescences of E. castrense. A possible explanation for why C. howelliana only flowered in N. leucocephala during 2012 is that during the 2013 N. leucocephala finished flowering much earlier in the season, long before C. howelliana began to produce flowers. However, the reasons for the phenological differences in N. leucocephala are unknown.
Of the two preferred host plant species, E castrense is a biennial and therefore has a longer life span than most other vernal pool plants which have an annual life cycle
(Baldwin et al. 2012, Whitham 2006). Eryngium castrense germinates while the vernal pool is still inundated and does not flower until most of the other vernal pool plants have already finished their life cycle. Navarretia leucocephala finishes flowering in
45 conjunction with many other vernal pool plant species and does not have as long of a life span as E. castrense (Baldwin et al. 2012, Whitham 2006).
It seems possible that E. castrense is a preferred host due to its long life cycle.
This would provide C. howelliana with a host for the duration of its life cycle allowing fewer resources to be spent on searching for a suitable host multiple times. Another possible reason for E. castrense preference is that it produces flowers after most other vernal pool plants have finished flowering. It also seems possible that C. howelliana produces flowers within inflorescences of E. castrense and N. leucocephala because it has easier access to pollinators that are otherwise attracted to these two host plant species.
However, the pollination mechanism of E. castrense is unknown (U.S. Fish and Wildlife
Service 2005). Research on pollinator relationships with C. howelliana and the two preferred host plant species would be interesting.
C. howelliana Removal Plots
In the plots where C. howelliana was removed, there was a significant decrease of plant species richness compared to plots where C. howelliana was not removed (Table 3).
However, there was no single plant species that showed a significant trend towards being absent in C. howelliana removal plots. A possible explanation for this is that most plant species on average showed a higher percent cover in C. howelliana present plots, but this did not become significant until all plant species were considered on one model.
46
Therefore, C. howelliana presence does not just create a vernal pool where one plant
species has a higher likely hood of being present.
Eryngium castrense was the only plant species that significantly decreased when
C. howelliana was present. During the last three sampling periods, the portions of C.
howelliana on plant species other than E. castrense and C. howelliana tissue connecting
it between individual host plants withered. This resulted C. howelliana being
concentrated solely on E. castrense hosts. Following this, C. howelliana flowered within
E. castrense inflorescences. This heavy infection of E. castrense near the end of the C. howelliana lifecycle is congruent in time with the decline in the percent cover of E. castrense during the last three sampling periods.
Rainfall in 2013 for California was much lower that 2012. Rainfall in 2012 was just around average. Decreased rainfall in 2013 lead to shorter inundation times for the vernal pool compared to 2012 (Bauder 2005, Graffis personal observation). There were likely some vernal pool plant species present in the seed banks that did not germinate because they require longer periods of inundation (Emery et al. 2009). An example of this pattern could be observed in the deepest pool that was sampled from for this experiment.
This pool was inundated for two weeks longer in 2012 than in 2013. In the center of this pool, Isoetes orcuttii was present in 2012 only. If the variation between a low precipitation year and an average precipitation year can cause a difference in the plant species richness in a vernal pool, than there might be a greater difference in the plant species richness in a low and a high precipitation year.
47
It would be interesting to see if C. howelliana has a different, or even greater,
effect on the plant community in a high or average precipitation year. It has been shown
that differing environmental conditions can effect host-parasite interactions and co-
evolution (Vale et al. 2008, Wolinska and King 2009). Rainfall specifically has been shown to alter host-parasite interactions. For example, Blue Palo Verde (Cercidium
floridum) mortality was shown to be correlated to Desert Mistletoe (Phoradendron
californicum) infestation during severe drought in the Mojave Desert (Spurrier and Smith
2007). Therefore, it is possible that C. howelliana would interact with hosts and the
vernal pool plant community in a different manner when different extremes in rainfall
occur between years.
Nararretia leucocephala did not exhibit different percent cover between the C. howelliana removal and present plots at any point in time (Table 10). This might be explained by the disjunction in 2013 on the flowering times of C. howelliana and N. leucocephala. Flowering time seems to be important because the decrease in E. castrense percent cover was congruent with when C. howelliana began producing flowers within the inflorescences of E. castrense. There were no observations in 2013 of C. howelliana producing flowers within the inflorescences of N. leucocephala. However, in 2012 many
N. leucocephala individuals were observed with C. howelliana flowers in their inflorescences. It may be that decrease rainfall and vernal pool inundation time lead to an earlier flowering time for N. leucocephala. This change in flowering time could lead to
C. howelliana not being able to produce flowers within N. leucocephala inflorescences.
48
Vernal Pools without C. howelliana Present
The trend of highest plant species richness in vernal pools with C. howelliana
present, intermediate plant species richness in C. howelliana removal plots, and lowest
plant species richness in vernal pools with C. howelliana naturally absent (Figure 6),
might be partially due to altered grazing regimes and partially due to the presence of C.
howelliana. Within the area of Beale Air Force Base that was used in this research, only
one section in the south western corner had vernal pools without C. howelliana naturally present. Cows were present during the whole sampling period in this south western section. In vernal pools where there was C. howelliana naturally present the cows were not present after April 31. Visibly the vernal pools with a longer cow presence had a large portion of inflorescences from the vernal pool plants consumed by cows, an increase in density of cow scat, and much more disturbed and compacted soil. Due to the difference in the grazing periods between the vernal pools with and without C. howelliana present, it cannot be said whether the observed increase in plant species richness in vernal pools with C. howelliana naturally present is due to the lack of C. howelliana in other vernal pools or due to the difference in grazing regimes.
It is possible that different grazing regimes did not have a significant effect on the
plant species richness of a vernal pool. If this is the case than the C. howelliana removal
plots are not showing the full effect of C. howelliana removal because the seed bank
present in those locations is reflective of a vernal pool with C. howelliana naturally
present. It could possibly take many years of C. howelliana removal to obtain a plant
49
species richness as low as a vernal pool where C. howelliana is not naturally present.
This would explain why the vernal pools without C. howelliana naturally present have
lower plant species richness than C. howelliana removal plots. Further research would be
needed to distinguish between the effects of different grazing regimes and the presence or
absence of naturally occurring C. howelliana in a vernal pool.
Other Parasitic Plants and Management Implications
Castilleja campestris, a hemiparasitic plant, is also endemic to California vernal pools. It does inhabit other types of wetlands, but is mostly confined to vernal pool habitat (Baldwin et al. 2012). A future study could examine the effects of holoparasitic
(C. howelliana) and hemiparasitic (C. campestris) plants on vernal pool plant communities. Castilleja campestris might not have as large an effect on the vernal pool plant community because of lower densities and less reliance on host plant carbon.
Considering the rampant loss of vernal pool habitat in recent years (Holland &
Jain 1988; Holland 1998), C. howelliana is another important consideration that should be taken when trying to maintain or increase species richness in a managed vernal pool habitat. Inclusion of C. howelliana in created or mitigated pools would function to maintain a higher level of plant species diversity over time. This could contribute to the overall success of a vernal pool management area.
This research also contributes to creating a more complete understanding of how parasitic plants interact with the communities around them. Cuscuta howelliana is
50 another example of a parasitic plant that has a positive effect on plant species diversity by parasitizing an abundant host. In this way the hypothesis that C. howelliana increases plant species diversity in vernal pools was supported. Due to the fact that there are numerous other mechanisms for maintaining vernal pool plant community diversity, it cannot be said that E. castrense is competitively dominant unless C. howelliana is present.
Cuscuta salina functions in a similar manner in coastal salt marshes by parasitizing the competitively dominant Salicornia virginica. However, C. salina also induces a cycling of plant species in a patch through time as S. virginica patches die following infection (Pennings & Callaway 1996). It would be interesting to determine if there is another level of complexity to the C. howelliana effects on the vernal pool plant community that functions in a similar manner. Due to the annual life cycle of communities in a vernal pool, any possible cycling of plant species due to C. howelliana presence would probably take place at the scale of years.
51
CONCLUSION
This study provides strong support that C. howelliana has an influence in shaping
the vernal pool plant community it lives within. Cuscuta howelliana presence was related
to increases in plant species richness, consistent with what is expected from the effects of a keystone predator. Cuscuta howelliana preferentially parasitized an abundant host (E.
castrense) and decreased that host’s presence. By this mechanism, more habitat was
made available for other plant species to become established, thus increasing plant
species diversity in a vernal pool. The presence of C. howelliana in a vernal pool also
was correlated with a higher total plant cover. The mechanism behind increased total
plant cover in a vernal pool with C. howelliana naturally present is unknown. This may
be connected to longer cow grazing times, not the absence of naturally occurring C.
howelliana from a vernal pool.
This research contributes to the body of research that parasitic plants are
important contributors to the maintenance of diversity in the communities they inhabit.
Therefore, interactions among species, including parasitic plants, needs to be considered
in restoration and management of California vernal pools. Consideration of C. howelliana
in management practices is important. Research into long term cycles or trends induced
by C. howelliana on its associated vernal pool plant species would be interesting to
investigate and compare to how other parasitic plants function.
52
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