CALIFORNIA STATE UNIVERSITY, NORTHRIDGE
THE ROLE OF LIFE-HISTORY TRAITS, TRADEOFFS, AND HABITAT IN THE
RARITY OF SANTA MONICA MOUNTAINS DUDLEYA SPECIES
(CRASSULACEAE)
A thesis submitted in partial fulfillment of the requirements
for the degree of Master of Science in Biology
by
Ann Dorsey
December 2009
The thesis of Ann Dorsey is approved:
______________________________________
Paula Schiffman, Ph.D.
________________
Date
______________________________________
Peter Edmunds, Ph.D.
________________
Date
______________________________________
Paul Wilson, Ph.D., Chair
________________
Date
California State University, Northridge
ii
ACKNOWLEDGEMENTS
This project would not have been possible without the help of many
people. The most noteworthy are: my advisor, Paul Wilson, who helped and
guided me throughout this project, my other thesis committee members, Paula
Schiffman, Lawrence Talbot (who helped in the early stages and after the first
draft), and Peter Edmunds (who helped in the later stages); the staff members at
the CSUN Botanic Gardens, Brenda Kanno and Brian Houck, who gave me
advice and a home for the study plants; all of the staff at Santa Monica Mountains
National Recreation Area who helped with this project especially regarding
showing me where to find the Dudleya; Stephen McCabe who shared his vast
knowledge of Dudleya with me; and Steven Norris at CSU, Channel Islands, who
made it possible to use the campus as one of my research locations. This project
was also greatly assisted by grants from the Western National Parks Association
and a Thesis Support Grant from the Office of Graduate Studies at CSUN.
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TABLE OF CONTENTS
Signature page..................................................................................................................... ii
Acknowledgements............................................................................................................ iii
Abstract .............................................................................................................................. vi
Introduction..........................................................................................................................1
Materials and Methods.......................................................................................................12
Study sites ..............................................................................................................12
Traits of rare versus common species....................................................................12
Habitat dependence: Coastal and inland gardens...................................................16
Data analysis ..........................................................................................................18
Results................................................................................................................................22
Traits of rare versus common species....................................................................22
Habitat dependence: Coastal and inland gardens...................................................30
Discussion ..........................................................................................................................38
Life-history tradeoffs .............................................................................................39
Environmental dependence of species’ prevalences..............................................42
Conclusion .............................................................................................................45
Literature cited ...................................................................................................................48
Appendix A: Interpretive background on Dudleya............................................................51
Appendix B: Nested ANOVAs and correlations ...............................................................55
Appendix C: The brick wall garden...................................................................................57
Appendix D: More information on coastal versus inland gardens ....................................62
Appendix E: Watering treatments......................................................................................65
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Appendix F: Differences between confusable taxa ...........................................................77
Appendix G: Management implications and recommendations........................................83
v
ABSTRACT
The Role of Life-history Traits, Tradeoffs, and Habitat in the Rarity of Santa Monica
Mountains Dudleya Species (Crassulaceae)
by
Ann Dorsey
Master of Science in Biology
In this study, life-history traits, tradeoffs in those traits, and habitat characteristics
of rare and common species were compared in an attempt to explain differences in
species distributions. The nine Dudleya species occurring in and around the Santa
Monica Mountains were studied. Five are rare narrow endemics with small localized
ranges, one is rare with an intermediate range, and three are common with broader
ranges. Life-history traits were studied in wild populations and in plants grown from wild
collected seeds. Habitat characteristics were recorded in two or three populations of each
study species. Differences that could explain why the rare species have smaller
distributions than the common species were found in aspects of growth, reproduction, and
habitat specialization. In regard to life-history traits and tradeoffs, rare species grew to a
smaller size and reproduced earlier than common species. The small body-size of the rare
species was correlated with smaller reproductive outputs than the larger-bodied common
species. The rare species also tended to have lower seedling survival. Reproductive
output and survival affect population size, persistence, and dispersal, all of which affect
vi
species distributions. The habitat requirements of the study species differed in terms of
co-occurring vegetation, geology, and microclimate, with the rare species being more
restricted compared to the common species. To further understand how habitat plays a
role in limiting species distributions, the nine species were grown in an inland garden and
in a coastal garden. Plants of all species grown in the inland garden were smaller in size
than those in the coastal garden. Moreover, the growth disparity between plants in the
two gardens was greatest for the rare species. The rare species have a lower tolerance for
hot dry conditions compared to the common species. In the Santa Monica Mountains
region, the habitat conditions required by the rare species are not as prevalent as those of
the common species. Differences in life-histories constrained by tradeoffs affect the
prevalence of the species, as well as specialization on rare habitats.
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Introduction
Evolution is a dance between the influences of genes and the environment sorted
at different scales in time and space with different processes working at each scale. Willis
and Whittaker (2002) and Whittaker et al. (2001) synthesized the different scales in time
and space with the ecological processes that occur at those scales. At the global scale,
over a span of 10 to 100 million years, evolution is shaped by processes such as sea level
changes and plate tectonics. At the continental scale, over 1 to 10 million years, mountain
building, aridification, and glacial cycles affect species richness and the distribution of
major lineages across continents. At the regional scale, over tens of thousands of years,
water-energy dynamics and climate influence the overlap of species ranges across large
geographic areas within continents. On the scale of a landscape over hundreds of years,
soils and topography are important to the turnover of species within a community and
species richness between adjacent communities. Finally, at the local scale, individuals
and groups of individuals living approximately at the same time vie against one another
for resources, thereby making habitat structure, disturbance, and ecological interactions
agents of selection. These delineations of processes into a given scale are not absolute.
Processes at a higher scale can affect those at a lower scale and visa versa. Also,
processes at different scales may have a combined effect.
Levin (2000) proposed that as species evolve they pass through four stages:
origination, expansion, differentiation, and decline to eventual extinction. This passage is
unique for each species and is affected by its ability to disperse, interactions with other
organisms, habitat conditions over time, ability to adjust to environmental change,
genetic variation, and developmental flexibility. A species’ geographic range changes as
1
it passes through these stages. It is defined by interactions between the species’ traits,
particularly their life-history, demographic, and dispersal characteristics, as well as
resource requirements and environmental tolerances. Environmental conditions,
especially the features that vary in space and time limiting population size and
distribution, also have an impact. The particular environmental conditions that restrict a
species’ distribution and abundance are unique to it and are expressed in the inability to
survive and reproduce in habitats with different sets of conditions. When there are many
conditions that limit a species, the places where it can live will be few and widely
separated (Brown et al. 1996).
The longevity of a species (how quickly it passes through the four stages) can be
affected by its characteristics and range size. Characteristics that can reduce the chances
of extinction are (1) life-history traits that allow for a rebound in population size
following a harmful environmental change, (2) high dispersal and recruitment ability that
allows the species to recolonize an area after local extinction, and (3) being a generalist
as opposed to a specialist because generalists tend to be locally abundant and
geographically widespread (McKinney 1997). Species with large geographic ranges and
population sizes tend to survive for longer than species with small ones as a consequence
of one or a combination of the following factors: environmental and demographic
stochastity, population fragmentation, the Allee effect, inbreeding depression, or reduced
genetic variation within populations (Gaston 1994, Kruckeberg and Rabinowitz 1985).
Differences between species in characteristics that affect population persistence and
range size can lead to some species becoming rare and others common. Specifically,
2
species distributions can be impacted by relationships between life-history traits and the
availability of a species’ habitat.
One evolutionary process that can affect species’ distributions is the expression of
tradeoffs between life-history traits. In a review of life-history literature, Stearns (1992)
discusses the role of tradeoffs in constraining evolution. Life-history traits include size at
birth, growth pattern, age at maturity, size at maturity, number, size and sex ratio of
offspring, age and size-specific reproductive investment, age and size-specific mortality
schedules, and length of life. Tradeoffs occur when there are linkages between traits such
that the simultaneous evolution of two or more traits is not independent. Nonindependence can ensue from physiological limitations such as energy resources being
finite. For example, there might be a tradeoff between rapid growth when small versus
the capacity to survive to an older age. Rapid growth at a small size is favored because
reproduction at a larger size leads to a greater reproductive output, but putting energy into
rapid growth instead of storage decreases the chances of surviving to reproduce later in
life (Metcalf et al. 2006). The allocation can be depicted as trading off within an
individual, but tradeoffs are manifested among individuals as they come to differ (Stearns
1992). Some individuals may put more energy into rapid growth when small, while
others put energy into storage when small. Divergent populations that persists in different
habitats may have one trait (rapid growth) selected for in one habitat type and the other
(energy storage) in another habitat (Levin 2000). At the macroevolutionary level, over
time, the selection of the different traits in the different populations could lead to the
evolution of new species. Some species within a genus may express traits at one end of a
tradeoff envelope (rapid growth but poor energy storage) and other species the other
3
(good energy storage but slow growth). The traits involved will be negatively correlated.
Though both traits in a tradeoff may be adaptive, one may lead to greater fitness than the
other. This, in turn, could lead to distributional differences between the species (Levin
2000). Beyond the life-history traits of the now divergent species, there will also be other
modifications because the species will have adapted to the different habitats in which
they live.
Habitat conditions that determine which species are found at a site can be biotic or
abiotic. Biotic examples include other plant species, herbivores, pollinators, and parasites
(Kruckenberg and Rabinowitz 1985, Stebbins 1978). Abiotic conditions include edaphic
conditions, temperature, rainfall, and day length (Levin 2000). A species will be able to
live in some range of these conditions and not in others. An example of this for biotic
conditions would be the presence of other plant species. They can limit the distribution of
a given species either because of competitive exclusion (Ackerly 2003) or because of
facilitative associations (Kruckenberg and Rabinowitz 1985). An abiotic example could
occur in an environment characterized by gradients of conditions (e.g. soil moisture
content). Species along this gradient will have traits that allow them to be most
competitive along a part of this gradient. They will not be able to perform well across the
entire range because of lack of physiological tolerances to some of those conditions,
which limits where they can occur (Cavender-Bares et al. 2004).
Species in the genus Dudleya exemplify these processes in which diversification
has been seemingly constrained along tradeoff envelopes and by differences in habitat
with concomitant effects on the geographic expanse of the resulting species. The species
to be compared are nine terminal taxa of Dudleya that occur in and around the Santa
4
Monica Mountains (located just west of Los Angeles, California: Dorsey 2007, Appendix
A). Taxonomists have been inconsistent as to whether all these terminal taxa are to be
treated uniformly at the rank of species or in some cases ranked as subspecies or even
synonomized, but for the rest of this thesis they will all be called “species”. Although
some of the characteristics of the rare species may be consequences of rarity and others
causes (Kunin 1997, Gaston 1994), no attempt is made to differentiate between
consequences and causes. Also, the terms “distribution” and “prevalence” will be used to
describe the relative abundance of the species – how many and how large the populations
are and how those populations are arranged geographically.
A few key characters of the nine species are introduced in Table 1. Of the nine
species, five are federally listed as threatened, and have distributions restricted even
within the Santa Monica Mountains. One species, D. b. blochmaniae, is rare but has no
legal status; it has a range size intermediate between the listed species and the common
species. The remaining three species are common, occurring from as far north as
Monterey County to as far south as Baja California.
A preponderance of Dudleya species, over half of the 44 treated in The Jepson
Manual, are said to be uncommon, rare, threatened, or endangered (Bartel in Hickman
1993). There are many factors that could explain this. A brief review of the evolution of
Dudleya sets the context. Most Dudleya species live within a few miles of the Pacific
Ocean from Baja California to southwestern Oregon, with a few having ranges that
extend much farther east. This coastal terrain was formed by the movement of three
tectonic plates. Going back 30 million years, scattered pieces of land that were part of the
Farallon Plate came into contact with the North American Plate, and then about 27
5
million years ago this aggregate was pushed against the Pacific Plate. The resulting
landmass consisted of a very complex topography made from different types of rocks,
facing different directions resulting in many different types of habitats. The major
lineages of Dudleya are believed to have originated here (starting about 5.5 million years
ago), then diversified on the Pacific Plate, i.e., west of the San Andreas fault (Uhl 2004,
1994). Less than 3 million years ago, summer rains ended along the coast of California
because of shifts in glacial climatic cycles and ocean circulation, and the rise of
mountains along the coast. Only plants that had traits allowing them to tolerate summer
drought persisted (Ackerly 2003). Dudleya species with their succulent leaves and CAM
photosynthesis were able to live in local sites that were sheltered from the worst of the
summer heat. The mountain ranges running along the coast of California created very
different cismontane and transmontane climates (Stebbins 1978). The coastal
predominance of Dudleya (Uhl 2004, 1994) could be because of this climatic difference.
The varied topography of the coastal mountains and multitude of soil types derived from
the many different geological formations allowed for the creation of pockets of unique
environments (Stebbins 1978) contributing to the very local distribution of many Dudleya
species (Uhl 1994).
The prevalence of the conditions a species is adapted to can determine how
common it is (Gaston 1994, Burgman 1989, Kruckeberg and Rabinowitz 1985). The rare
Dudleya species included in this study have small geographic ranges, narrow habitat
specificity, are locally abundant in the specific habitats where they occur, and are
considered narrow endemics using the criteria of Rabinowitz (1981). The theme to be
explored below is that Dudleya species’ distributions are constrained by life-history
6
tradeoffs at a macroevolutionary level and by habitat at a microevolutionary level. In
particular, adapting to reproduce quickly and making the best of an unusual rock type
may keep a species that has specialized from expanding beyond a few sites, in contrast to
a species that has adapted to delay reproduction and grow to be larger and more stressresistant.
This thesis, then, explores possible reasons for differences in the prevalences of
the nine Dudleya that live in the Santa Monica Mountains and surrounding areas. Two
topics are woven throughout the thesis. First, traits of rare versus common species were
contrasted to establish in which traits, if any, there were differences. The traits were
correlated against one another to determine which were involved in tradeoffs. The
hypotheses tested were that rare species would be inferior in regard to some aspect of
survivorship or reproduction, but would be better in life-history traits that were
accentuated as opposed to those that were traded off. Also, aspects of habitat were
contrasted. Data were collected on the microenvironments in which the nine species
occur. These habitat characteristics were compared to ascertain, as hypothesized, if rare
species occurred in more specialized habitats than common species. Second, the habitat
dependence of variations in performance among species is presented. Specifically, the
hypothesis tested was that rare species would be more impacted than common species by
harsh inland conditions compared to conditions where there is a coastal influence.
Differences in performance on the coast and inland were correlated with more
conventional life-history traits. For instance, the growth of individuals at one location
was compared with coastal and inland reproduction to determine if the disparity between
sites was a consequence of a tradeoff.
7
Table 1. Rarity and distinctiveness of nine Dudleya taxa.
Abbreviation
Subgenus epithets
D. Hasseanthus
bloc
blochmaniae subsp.
blochmaniae
Rarity
Distributiona
Rare but not San Luis Obispo Co. to
listed
northern Baja California
along coast
Petal charactersb
White, ± yellowish green
at the base, red on the
keel, 2.5-3.5 mm wide
Pale yellow sometimes
red-lineolate on the keel,
2-3.5 mm wide
Lemon yellow with a
touch of green along the
midrib, 2.5-4 mm wide
Slightly orange yellow
often marked with red,
2.5-3.5 mm wide
Bright yellow, 2-2.5 mm
wide
Other distinguishing
charactersb
Rosette leaves vernal,
resprouting from a corm
D. Dudleya abramsii
subsp. parva
parv
Threatened
Ventura Co.
D. Dudleya verityi
veri
Threatened
Ventura Co.
D. Dudleya cymosa
subsp. marcescens
marc
Santa Monica mts
D. Dudleya cymosa
subsp. ovatifolia
ovat
USFWS
threatened;
CA rare
Threatened
D. Dudleya cymosa
subsp. agourensis
agou
Threatened
Santa Monica mts
D. Dudleya
lanceolata
LANC
Common
D. Dudleya
caespitosa
CAES
Common
D. Dudleya
pulverulenta subsp.
pulverulenta
PULV
Common
Santa Barbara Co, to
Rosette leaves green or
northern Baja
glaucous
California
Orange-yellow to red, 2.5- Plants are clonal with up
Monterey County to Los
Angeles County, near the 5 mm wide
to 150 rosettes
coast
San Luis Obispo Co. to
Red & glaucus on keel, 2-4 Rosette leaves chalkycentral Baja California
mm wide
pulverulent
on coastal ranges
(ornithophilous)
Santa Monica mts
Bright yellow,
occasionally glaucous
along the midrib
Yellow to red, 2.5-5 mm
wide
a
Rosette leafless in summer Conejo
volcanic
breccia
Plants are clonal with 25- Volcanic rock
100 rosettes
outcrops
Rosette leaves wither in
the summer
Sheer volcanic
surfaces
Rosette leaves green, not
glaucous, reddish on the
underside
Rosette leaves glaucous
Sedimentary
conglomerate
Distribution from Moran 1951 , Nakai 1983 , Nakai 1987, for a more detailed description of habitat and range see Dorsey 2007.
Floral and other distinguishing characters from Moran 1951, Nakai 1983 , Nakai 1987, Aigner 2004, and pers. obs.
c
USFWS 1999, Bartel in Hickman 1993.
b
8
Associated
geologyc
Rocky clay or
serpentine soil
Pleistocene
dissected
gravels
Various rocky
slopes
Various rocky
sites
Rocks,
mineral soil
Materials & Methods
Study sites
Seeds were collected and habitat observations were made in the Santa Monica
Mountains and surrounding areas in two counties. Sites in Los Angeles County were:
Malibu Creek State Park (34.103o N, 118.734o W), Cornell Corners (34.110o N, 118.775o
W), Semler Open Space (34.146o N, 118.806o W), and Seminole Hot Springs (34.107o N,
118.791o W). Sites in Ventura County were: Joel McCrea Wildlife Preserve (34.236o N,
118.859o W), Wildwood Regional Park (34.219o N, 118.919o W), Rancho Potrero Open
Space (34.167o N, 118.946o W), Thornhill Broome Beach (34.084o N, 119.036o W), Leo
Carrillo State Park (34.046o N, 118.928o W), Conejo Mountain (34.188o N, 118.984o W),
and California State University, Channel Islands (34.162o N, 119.043o W).
Traits of rare versus common species
Field observations – Twelve sites were studied, each with 1 to 3 species of
Dudleya. At the time of fruit collection, data on the parent plant’s number of
inflorescences, tallest inflorescence height, number of fruits, longest leaf length, and
number of leaves were recorded. Information was noted about the habitat the Dudleya
were growing in: any vegetation the plant was growing in close proximity to, the distance
to the nearest neighbor of the same species, slope, aspect, and if any shading was
provided by trees, cliffs, etc.
Seed collection – Fruit ripeness was monitored from June through August 2005.
Fruits were collected from mid-July through the end of August when they looked dry but
before the follicles had opened. Three randomly chosen fruits each were collected from
12
30 randomly chosen individuals, from 2 or 3 populations of each species (three for D. b.
blochmaniae, D. lanceolata and D. p. pulverulenta, and two for D. a. parva, D. verityi, D.
c. marcescens, D. c. ovatifolia, D. c. agourensis and D. caespitosa). Fruits were cut from
the inflorescences and placed individually in labeled envelopes.
Collection deviations – Many of the D. p. pulverulenta had been partially eaten by
deer or rabbits so only plants that had intact inflorescences and leaves were used for fruit
and data collection. Only one fruit per plant was collected from D. c. marcescens and two
fruits from D. c. ovatifolia because of their protected status. Leaf number, and nearest
neighbor distances may have been underestimated for D.verityi and D. caespitosa
because individual plants are capable of forming multiple rosettes. Only the main rosette
was studied. Also, rosettes of the same individual may have been considered as belonging
to a neighbor. At the time of seed collection leaves were not present for D. b.
blochmaniae and were not present on all D. a. parva plants. Therefore, leaf-related data is
missing for these two species. For D. p. pulverulenta and D. lanceolata, in some cases,
the individuals were too sparsely spaced to include five neighbors. In addition, it was not
always possible to distinguish D. b. blochmaniae plants from their neighbors, because at
the time of collection only the inflorescences were present. It was assumed each
inflorescence was a separate plant, but later observations revealed there could be multiple
inflorescences. Nearest neighbor distances, therefore, were underestimated for this
species. Although precautions were taken to ensure the purity of the species at the time of
data collection, some of the D. c. marcescens and D. c. ovatifolia individuals’ data and
seeds collected may actually be from Dudleya hybrids.
13
Seed preparation – Fruits were stored in envelopes at room temperature and
allowed to dry fully for at least one month before the seeds were counted. Follicles were
held over a piece of white paper inside a box lid. Seeds were shaken loose as much as
possible, then follicles were broken open over the paper to release the remaining seeds.
Non-seed material was removed. Seeds were picked up by gently placing an index finger
over them. Seeds on the finger tip were counted and placed into a labeled envelope with
the corners folded up to prevent the loss of seeds. Seeds from the fruits of the same
individual were placed in the same envelope until there were 30 seeds. This process was
repeated for a second envelope. Any seeds remaining were placed in a third labeled
envelope. All seeds of all collected fruits were counted. Seeds were stored in a
refrigerator.
Seed projected area – Seeds from a randomly chosen subset of individuals and
fruits of each species were measured using the ocular micrometer of a dissection
microscope. Seeds were placed in a small box lid on a piece of white paper and were
placed under the microscope for observation. The largest (presumably healthiest) five
seeds were chosen for measurement in order to include only viable seeds. Chosen seeds
were picked up on a piece of transparent tape and taped onto an index card for
measurement under the microscope. Length and width of each seed were recorded. Once
all of the seeds were measured, ocular units were converted to millimeters. Projected area
was estimated as the surface area of an ellipse (SA = πr1r2).
Seed sowing and seedling care – On 20 December 2005 sixty seeds of each
individual for all nine species were surface sown in 4” plastic pots (30 seeds per pot, 2
pots per mother plant). Not all mother plants of all species had 60 seeds, in which case all
14
the available seeds were sown, 1/2 in one pot and 1/2 in the other. A few individuals
produced no seeds (one individual each of D.verityi, D. c. ovatifolia, D. lanceolata, and
D. caespitosa). The potting mixture consisted of 2 parts sunshine potting mix, 2 parts
vermiculite, and 1 part perlite. Vermiculite was also sprinkled over the top of the filled
pots before the seeds were sown. Pots were labeled as to species and mother. After the
seeds were sown, they were watered with low water pressure to avoid the spread of seeds
from one pot to the next.
Pots were kept in flats in a greenhouse. The flats were rotated 180o and along the
bench weekly. The potting mix was gently watered as necessary to keep the mixture
moist. Once the seedlings had emerged and were established, the mixture was allowed to
dry somewhat between waterings to prevent fungus growth, the proliferation of fungus
gnats, and to harden the plants. Seedlings were fertilized the first time 13 January and
were fertilized weekly until 30 March 2006. The first fertilization was with 1/4-strength
Miracle Grow (15-30-15). The rest of the fertilizations were with Grow More (20-20-20)
at alternating strengths 1/4 or 1/3 until 17 March, at which time the strength was
increased to 1/2. The final fertilization was 25 April after all plants had been transplanted
and placed outside in a shade house.
Germination and seedling survival – Numbers of sprouted seedlings were counted
from the first week after sowing, 27 December 2005, weekly until 1 February 2006 when
the seedlings became too crowded to accurately count their numbers. Seedlings were
transplanted once most or all of the individuals in a pot had 2 to 3 post-cotyledonous
leaves. Transplantation started 20 February 2006 and continued until 21 April 2006. Most
of the transplantation occurred in April. Final counts of seedlings were taken at the time
15
of transplantation. Seedlings were transplanted individually into labeled plastic 4” pots.
Once transplanted the seedlings were watered. Eleven of the biggest, healthiest looking
seedlings (siblings) from each mother plant were transplanted into pots. The seedlings
transplanted into pots were randomly assigned to 1 of 6 treatment groups or to be extras.
One set was grown between bricks. One set was grown in a coastal garden, and another in
an inland garden. The remaining three sets were assigned to three watering-treatments
(Appendix E), which in the present context are only relevant in that they were used to
measure each species’ proclivity to bolt. Plants were allowed to acclimate for
approximately one month before the first experimental treatments commenced.
Brick wall garden – A set of plants were grown with the roots sandwiched
between vertically stacked bricks. This mimicked the way Dudleya often grow in nature,
inside cracks in rock outcrops. It also facilitated the measurement of roots and shoots of
simultaneously established plants. During planting, drip irrigation lines were installed.
Watering was more generous than it would have been in nature but was still seasonal.
Plants were harvested after two summers. Roots were dried separately from shoots.
Details are given in Appendix C.
Habitat dependence: Coastal and inland gardens
Site descriptions – Two gardens were planted in different near-natural
environments, inland and coastal, within the naturally occurring range of the common
species. The coastal garden site was in Zuma Canyon (34.106o N, 118.819o W), a site that
in late spring frequently receives maritime fog and cloud cover. The inland garden was
inland of the first ridges in the hills overlooking the San Fernando Valley to the north
16
(34.118o N, 118.585o W). Plants at the coastal location were planted out 21 June 2006.
Plants at the inland location were planted out 7 June 2006 and (only a few) on 9 June
2006. Three plots per garden location, roughly 6.5’ × 3.5’, were dug to a depth of 4 – 6”.
A sheet of 6’ × 3’ hardware cloth was placed on the bottom of the plot. Plants of all the
species were placed in random order in the dug out area on top of the hardware cloth. The
potting mixture in the pots was retained in the garden so that the plants were close to the
same level as the surrounding ground. Individuals were placed next to each other in rows
of four. As each row was filled, the next row was put in place until a 6’ × 3’ area was
filled. Soil from the location was added to fill in gaps between plants as necessary.
Coastal plots contained 83 to 85 individuals each. Inland plots contained 80 to 88
individuals each. Exclosures (6’ × 3’ × 1.5’) constructed of 2 × 4s and hardware cloth
were placed over the plots to prevent herbivory. HOBOs were placed at each garden site
at the time the plants were planted out to record temperature, dew point, and humidity in
the coming year. The coastal garden was shaded by Platanus racemosa and Juglans
californica trees. The inland garden was shaded by Juglans californica trees.
Data collection – Plants were watered once they were planted out and weekly
thereafter for 4 weeks to allow them to become established in the gardens. After that,
they received only natural precipitation. Observations of the general condition of the
plants were noted every week from the time of planting to 20 August 2006 after which
time observations were made every two weeks. One month after planting, 4 plants in the
inland garden were lost to small mammals that had broken through the hardware cloth,
and some coastal garden plants lost outer leaves to pill bugs. This damage did not appear
to interfere with the plants’ growth. Flowers were cut off the inflorescences as necessary
17
to limit the amount of energy allocated to reproduction (Jongejans et al. 2006), control for
energy allocation differences between reproductive and non-reproductive individuals, and
to prevent the accidental introduction of Dudleya species to the sites. Every two months,
from June 2006 to June 2007, data were collected on the number of leaves, longest leaf
length, and number of inflorescences of each individual. Final size and reproductive data
were collected 12 November 2007 for the coastal garden and 10 November 2007 for the
inland garden. Coastal garden plants were removed 15-16 December 2007. Inland garden
plants were removed 24-26 November 2007. At the time of removal, plant roots were cut
just below the rosette, any dry inflorescence parts were removed, ink prints of the crosssectional area of the root crown below the leaves were made, and the rosettes were placed
into labeled paper bags. The bags were dried at 37.8o C for several months until weights
stopped decreasing.
Data analysis
Habitat and life-history data – Mixed-model nested ANOVAs were done
comparing rare and common species, and testing for significant differences among
species within rarity categories. The “rare” category included six species (except for leaf
data in which case it included four species) and the “common” category included three
species. These were done for nearest same-species neighbor distances, slope, degrees
from north, log longest leaf length, square root leaf number, log inflorescence height,
cube root fruit number, seeds per fruit raised to the negative one-sixth power, seed
projected area, arcsine percent germination, and percent seedling survival.
18
Germination and seedling survival – Germination percentages were estimated by
using the highest number of seedlings counted per individual divided by the total number
of seeds sown. Seedling survival percentages were estimated by multiplying the
probability of germinating by the probability of surviving from the germination stage to
the transplantation stage.
Reproductive output and percent bolting – Reproductive output was estimated by
multiplying the number of fruits produced on a given individual by the average number
of seeds per fruit on that individual. Species averages were then calculated. Percentage of
reproductive individuals for each species during the 1st, 2nd and 3rd springs after
germination were calculated by dividing the number of individuals with inflorescences in
each species in the three watering treatment groups by the total number of individuals of
that species in these groups.
Brick wall – Two variables were considered from the plants grown in the brick
wall. Total biomass dry weight was the sum of rosette biomass dry weight and root
biomass dry weight. Root-to-shoot ratio was the quotient of these two numbers, and used
as a measure of allocation.
Evidence of tradeoffs – Correlations among species were calculated. In some
cases, they did not include D. b. blochmaniae because many of the plants of that species
were not in evidence above ground for much of the year. Individual Pearson correlations
were done comparing (1) the percent of each species reproductive over three springs
(summed) with dry weights of plants grown in the brick wall garden (not including D. b.
blochmaniae), (2) the root-to-shoot ratios and the total biomass dry weights from the
plants grown in the brick wall garden (excluding D. b. blochmaniae), (3) the seed
19
projected area and the number of seeds per fruit for all study species, (4) the size and
reproductive output of all the study species except D. b. blochmaniae from plants
growing in the wild, and (5) seed projected area and percent of individuals that survived
to be seedlings for all species.
Differences between coastal and inland gardens – A variable indexing size was
calculated as log ([longest leaf length × number of leaves] + 1). This “leaf size” variable
was subjected to a repeated measures ANOVA in which site, rarity, and species-withinrarity were crossed with census date, “site” being the one coastal versus the one inland
garden location. For the variables measured at the end of the experiment, namely root
crown cross-sectional areas and rosette dry weights, split-plot ANOVAs were done
involving site, rarity, and species within rarity. The above analyses did not include D. b.
blochmaniae. The root crown cross-sectional areas of two plants (D.verityi #15 in the
inland garden and D. caespitosa #25 in the coastal garden) were winsorized because they
greatly exceeded the other values for that species.
Pearson correlations were used to compare a life-history variable and a coastal
minus inland difference to test for the presences of a tradeoff between these traits. For
leaf size, the date with the maximum differences between the coastal and inland gardens
was used. This difference was correlated against a measure of size from different plants,
the total biomass dry weight of plants grown in the brick wall garden. A Fisher’s exact
test was used to see if the percent of individuals that were reproductive for each species
in the coastal garden differed from those in the inland garden. The difference in percent
reproductive in the coastal and inland gardens was correlated against the total biomass
dry weight of the plants grown in the brick wall garden, not including D. b. blochmaniae.
20
Statistical caveats – In many analyses, the factor “rarity” is included. It consists
of three common species (D. lanceolata, D. caespitosa, D. p. pulverulenta) versus five or
six rare species (sometimes excluding D. b. blochmaniae). With such small sample sizes,
null hypotheses should be accepted cautiously, and even non-significant differences
noted as possibly representing a difference. Slightly more powerful are correlations in
which eight or nine species are used as data points. The eight or nine were treated as
independent even though these species are related at various phylogenetic levels.
Differences between the species or between rare and common groups could be because of
evolutionary adaptations required for survival in the unique microhabitats or because of
phylogenetic conservatism of the traits involved (Westoby et al. 1995). It is not clear
which of these causes may have influenced the study species. Another caveat is that there
was pseudoreplication in the analysis of the gardens (Hurlbert 1984). There were only
two gardens and the analyses were performed as if individual plants were replicates.
Given the difficulty of having multiple gardens of each type and the observable and
measurable differences between the gardens, the significance tests seem useful to check
for variance greater than the individual variance within species in a garden.
21
Results
Traits of rare versus common species
Life-history data – Appendix B and Dorsey (2007) give some growth and lifehistory information for each of the nine species. Briefly, longest leaf length ranged from
1.4 to 11.7 cm. The leaves of common species were significantly longer than those of rare
species (P = 0.009, F = 17.199, df 1, 5). The number of leaves ranged from 5 to 44.
Dudleya cymosa ovatifolia and D. c. marcescens, both rare species, had the fewest
number of leaves and D. p. pulverulenta, a common species, had the greatest number of
leaves, but differences between rare and common species were not significant (P = 0.149,
F = 2.910, df 1, 5). Inflorescences varied between 11 and 88 cm tall, with common
species having taller inflorescences than rare species (P < 0.001, F = 46.838, df 1, 7). The
number of fruits per individual ranged from 10 to 157. Rare species produced
significantly fewer fruits per individual than did common species (P = 0.008, F = 13.401,
df 1, 7). The numbers of seeds per fruit, ranged from 17 to 551, and were greater for
common species than for rare species (P = 0.031, F = 7.280, df 1, 7). Seed projected area
ranged from 0.185 to 0.487 mm2, with rare species generally producing smaller seeds
than common species (P = 0.009, F = 12.700, df 1, 7). Rare species tended to have a
greater number of individuals reproduce each spring than common species (Figure 1). In
the first and third springs more individuals of each rare species reproduced than of each
common species. In the second spring, most of the rare species had a greater number of
individuals reproduce than the common species. The exceptions were the summer
deciduous D. a. parva (97%) and D. b. blochmaniae (96%), which were equal to or
22
slightly less than D. lanceolata (97%), the common species with the greatest number of
reproductive individuals.
100
1st spring
90
2nd spring
% reproductive
80
3rd spring
70
60
50
40
30
20
10
0
bloc
n = 82
n = 82
n = 79
parv
veri
marc
ovat
78
78
73
90
90
88
84
82
79
75
74
74
agou LANC CAES PULV
90
90
88
87
87
87
87
87
87
78 1st spring
77 2nd spring
77 3rd spring
Figure 1. Percent of individuals of each species reproductive in each of three springs (2006-2008). Data
from plants in the three water treatment groups. The number of individuals with inflorescences was divided
by the total number of individuals for each species.
Survival – The survival of individuals of all of the study species to three different
stages of life were tracked (Figure 2). Survival to the germination stage ranged from 4380%. Of all of the stages, this was the one that showed the greatest decline in numbers of
surviving individuals. Survival to the seedling stage, age 2 to 4 months (just before they
were transplanted) ranged from 30-75%. After plants were transplanted very few died.
Survival to the end of the study (age ~ 2 years) ranged from 30-75%. Although there
were significant differences among species there were not between rare and common
species when comparing percent germination (P = 0.013, F = 10.875 and P = 0.252, F =
1.558 respectively, df 1, 7) and percent survival to the transplantation stage (P = 0.002, F
= 21.218 and P = 0.302, F = 1.239 respectively, df 1, 7).
23
100
80
% survivorship
LANC
parv
CAES
60
bloc
agou
veri
PULV
ovat
40
marc
20
Seeds
Germinated
Transplanted
End
Figure 2. Comparing species in terms of survival to different life stages. Seeds: number of seeds sown.
Germinated: maximum number of seedlings divided by number of seeds sown. Transplanted: probability of
seeds germinating multiplied by probability of survival from germination to transplantation. End:
probability of survival to transplantation multiplied by probability of survival from transplantation to the
end of the study (all groups).
Life-history tradeoffs – Correlations were calculated between life-history traits in
order to determine which were involved in tradeoffs. The brick wall biomass dry weights
were strongly negatively correlated with the sum of the percent of reproductive
individuals over three springs in the water treatments (r = -0.846, P < 0.01, n = 8: Figure
3A). Rare species were smaller and had more individuals reproduce than the larger
common species. Some traits were negatively related but not significantly. The
correlation of root-to-shoot ratios plotted against total biomass dry weight (roots plus
shoots) was negative and non-significant (r = - 0.438, P > 0.20, n = 8: Figure 3B).
24
B -0.2
3
parv
parv
LANC
-0.3
ovat
2.5
Reproduction over 3 springs
veri
marc
agou
-0.4
agou
marc
2
log(root:shoot)
A
LANC
1.5
1
CAES
CAES
veri
-0.5
-0.6
ovat
-0.7
-0.8
0.5
-0.9
PULV
r = -0.846, P < 0.01
0
-0.75
-0.25
PULV
r = -0.438, P > 0.2
0.25
0.75
log(dry weight, g)
-1
-0.75
1.25
C -0.3
-0.5
-0.25
0
0.25 0.5
log(root+shoot)
0.75
PULV
4.5
-1/6
-0.4
LANC
-0.45
-(Seeds/fruit)
log (reproductive output in wiild)
-0.35
-0.5
ovat agou
-0.55
marc
-0.6
veri
CAES
parv
bloc
r = -0.269, P > 0.20
-0.7
0.15
0.2
0.25
0.3
0.35
0.4
0.45
LANC
parv
70
CAES
65
bloc
agou
55
50
PULV
veri
ovat
40
35
30
marc
r = 0.792,P < 0.02
25
0.16
0.2
LANC
veri
3
marc
ovat
r = 0.860, P < 0.01
E 80
60
agou
parv
Seed projected area, mm2
75
CAES
4
3.5
-0.65
% Seedling survival
1.25
D 5
PULV
45
1
0.24
0.28
0.32
0.36
Seed projected area, mm2
0.4
0.44
25
2.5
-0.5
0.5
1.5
log(size in wild)
2.5
Figure 3. Signs of life-history tradeoffs and other relationships. A. Biomass dry weights of each species are
from plants grown in the brick wall garden. The percent of individuals of each species reproductive each of
three springs were summed. Data were from plants in the three water treatment groups in 2006-2008. B.
Root-to-shoot ratios are biomass dry weights of roots divided by that of rosettes. Root + shoot are biomass
dry weights of roots and rosettes added together. Data from plants grown in the brick wall garden. C.
Projected area of seeds was calculated using the length and width of the seeds and the formula for the area
of an ellipse. Number of seeds per fruit generally from 3 fruits of 30 plants growing in the wild in 2 or 3
populations were counted. D. Size was measured as the number of leaves times the longest leaf length.
Reproductive output is the number of fruits times the number of seeds per fruit. Data were collected from
30 plants of each species in 2 or 3 wild populations. E. Projected area of seeds was calculated using the
length and width of the seeds and the formula for the surface area of an ellipse. Seedling survival was
measured as the product of the probability of seeds germinating and of seedlings living to be transplanted.
26
Total biomass was involved in a life-history tradeoff with rare species being lighter and
common species heavier, but most of the species had similar root-to-shoot ratios ranging
from 0.28 to 0.55 (22 – 35% root). Dudleya a. parva, a species that dies back to a caudex
in the summer, had a disproportionately large root mass of 0.84 g (46% root). Dudleya p.
pulverulenta had a disproportionately large rosette mass of 0.13 g (11% root) and is one
of the large-bodied species with the greatest delay in reproduction. (There are no data for
D. b. blochmaniae for which root-to-shoot data are not applicable because they die back
to corms: Appendix C, Figure C-3). There was a non-significant negative correlation
between seeds per fruit versus seed size (r = -0.269, P > 0.20, n = 9: Figure 3C). Rare
species tended to have fewer seeds per fruit, the exceptions being D. c. agourensis as
compared to D. caespitosa, and rare species generally produced smaller seeds than
common species, the exception being D. p. pulverulenta, which produced the smallest
seeds. Other pairs of characteristics were not involved in tradeoffs and included size in
the wild (number of leaves multiplied by the length of the longest leaf) and reproductive
output (number of fruits multiplied by seeds per fruit) which were strongly positively
correlated (r = 0.860, P < 0.01, n = 7). Smaller sized rare species had smaller
reproductive outputs than larger sized common species (Figure 3D). Finally, seed
projected area and percent seedling survival were positively correlated (r = 0.792, P <
0.02, n = 9). Species with smaller seeds tended to have fewer individuals survive to the
seedling stage (Figure 3E). Similarly, seed projected area and percent germination were
positively correlated (r = 0.712, P < 0.05, n = 9). Species with smaller seeds tended to
have fewer individuals germinate. Correlations are treated in a more thorough fashion in
Appendix B.
27
Average distance to near neighbors
1600
A
1200
800
400
0
200
Degrees from north
B
150
100
50
0
c rv
ri rc at ou NC ES UL
blo pa ve ma ov ag LA CA P
V
Figure 4. Comparison of species for two microhabitat variables. A. Average distances (cm) from nearest
same-species neighbors for each species. The distances of the five nearest same-species neighbors were
measured for 30 individuals of nine species in 2 or 3 populations. The distances were averaged per
individual and then by species. B. The aspects of the substrate for 30 individuals of nine species in 2 or 3
populations. The data were then converted into degrees from north. For both variables, rare species were
not significantly different from common species, but there were significant differences among species.
Habitat data – The average distance to the five nearest neighbors (a measure of
population density) ranged from 6.3 to 501.4 cm, with the common species being the
sparsest and the rare species being the densest (Figure 4A). There was significant
variability among species (P < 0.001, F = 37.397, df 7, 261), but not between rare and
common species (P = 0.317, F = 1.160, df 1, 7). Slope of the substrate a given individual
was growing on ranged from flat (0o) to vertical (90o). There was no significant
difference between rare and common species (P = 0.807, F = 0.065, df 1, 7), but there
28
was significant variability among species (P = 0.003, F = 20.187, df 7, 261). Aspect of
the substrate a given individual was growing on ranged from 0 (directly north) to 180o
from north (directly south). Most individuals of both rare and common species grew on
substrates with aspects within 90o of north, but common species had more individuals
facing further away from north (Figure 4B). Of the forty individuals that faced greater
than 90o from north, only five were rare. They were D. c. ovatifolia individuals that faced
180o from north and are a special case in that they were shaded by trees and an opposing
rock face and so received little direct sun. Again there were no significant differences
between rare and common species (P = 0.417, F = 0.744, df 1, 7), although there were
among species (P = 0.001, F = 28.048, df 7, 261: Appendix B).
Habitat observations – Dudleya b. blochmaniae grew in shallow soil deposits on
rocks or rock outcrops and in patches of rocky soils surrounded by grasses. Co-occurring
vegetation included grasses, if sparsely spaced, and Dudleya verity, when growing on
rock outcrops, but the two species do not grow intermixed. Selaginella, mosses, and
lichens were also found on the rocks. If any shading was present, it was from rock
outcrops. Dudleya a. parva occurred on rocks (mostly) and in soil. The rocks often had
Selaginella growing on them. Co-occurring vegetation included grasses, if sparsely
spaced, and Selaginella. There was no shading other than by rock outcrops. Dudleya
vertiyi was found on rock outcrops with lichens, mosses, and Selaginella. Co-occurring
plants, growing peripherally, were sometimes other Dudleya especially D. b.
blochmaniae. The rock outcrops they were growing on provided the only source of shade.
Dudleya c. marsescens occurred on sheer rock faces. Co-occurring vegetation was often
mosses. Plants grew mostly in areas shaded by trees and with water nearby. Dudleya c.
29
ovatifolia grew on conglomerate rock formations mostly, but was found on other rock
types. There was little co-occurring vegetation other than mosses and lichens. Plants grew
in the shade of trees or canyons mostly with water nearby. Dudleya c. agourensis
occurred on rock outcrops or in patches of rocky soils surrounded by grasses. Plants were
found especially with Selaginella but mosses and lichens also co-occurred. The only
shading was provided by the rocks they grew on. Dudleya lanceolata grew in rocky soils
or soil deposits on rocks of various sorts. If growing on rock outcrops, they were
sometimes found with D. p. pulverulenta and in small numbers peripherally with D. c.
ovatifolia and D. c. marsescens. If growing on rocky soils they co-occurred with other
vegetation, predominantly Eriogonum fasciculatum and sometimes D. p. pulverulenta.
Some shading could be provided by rock outcrops or the co-occurring vegetation.
Dudleya caespitosa grew near the Pacific Coast on rocks or rock outcrops with soil
deposits. Co-occurring vegetation included Eriogonum fasciculatum and Yucca whipplei.
Dudleya p. pulverulenta also occurred in the same area. No shading, other than by rock
outcrops, was provided. Dudleya p. pulverulenta occurred mostly on rock outcrops but
was found in rocky soils also. When growing on rock outcrops in the less exposed more
north facing areas, other Dudleya species were present in the general area. Co-occurring
vegetation, when growing on more exposed rocky soils, was most often Opuntia littoralis
or O. oricola, often Eriogonum fasciculatum, and seldom Yucca whipplei. This species
may have received some shading from rock outcrops or nearby vegetation, but tolerated
full exposure and south facing slopes.
30
Habitat dependence: Coastal and inland gardens
Environmental data – From April through August, the coastal garden had cooler
temperatures and higher humidity than the inland garden (Figure 5). From September
through November, the temperature and percent humidity of both gardens were similar.
Plant size – In general, plants grew to be larger at the coastal garden than the
inland garden (Figure 6). The size changed through the seasons, increasing during the
growing season and decreasing when the plants showed signs of physical dormancy. All
species were smaller in the inland garden than in the coastal garden, but the disparities in
size were greater for the rare species than for the common species. This disparity was
greatest in late summer and fall when the weather was hot and dry. Using the species
other than D. b. blochmaniae, there was a significant difference in size, log([leaf number
× longest leaf length] + 1), between rare and common species in the two gardens over
time (date × rarity × site P = 0.038, F = 2.386, df 7, 42), between gardens over time (P <
0.001, F = 15.683, df 7, 42), between rare and common species over time (P = 0.011, F =
3.045, df 7, 42 ), over time (P < 0.001, F = 32.142, df 7, 42), between rare and common
species in the two gardens (P = 0.015, F = 11.335, df 1, 6), and between the gardens (P <
0.001, F = 106.834, df 1, 6), but only marginally between the rare and common species
(P = 0.074, F = 4.686, df 1, 6: repeated measures ANOVA given in Appendix D). The
rosette biomasses were greater for plants grown in the coastal garden than for those
grown in the inland garden (Figure 7A). Inland root crown cross-sectional areas were
smaller than coastal ones for the rare species (Appendix D). For common species coastal
root crown areas were smaller, except in the case of D. p. pulverulenta. Differences in
root crown sizes between the gardens were not significantly different for any of the
31
Temperature C (average 12-3 pm)
A
45
coastal
inland
40
35
30
25
20
15
10
% Humidity (average 12-3 pm)
B 100
90
80
70
60
50
40
30
20
10
0
0
2
J
4
6
8 10 12 14 16
week in garden
J
A
S
18 20 22
41 43 45
A
O
47 49 51
M
53 55 57 59 61 63 65
week in garden
J
J
A
S
67 69 71
73
O
N
Figure 5. Climate of a coastal and an inland garden over time. A HOBO was placed in each garden and readings were taken every 15 minutes. Data in the graphs
were taken from June through November 2006 and from May through December 2007. The readings from 12:00 pm to 3:00 pm were averaged. A. Temperature.
B. Percent humidity
32
3
coastal
A bloc
B parv
C veri
D marc
E ovat
F agou
G LANC
H CAES
2.5
inland
2
1.5
1
0.5
log(linear size +1)
0
3
2.5
2
1.5
1
0.5
0
3
I PULV
2.5
2
1.5
1
0.5
0
J J A S O N DJ F M A M J J A S O N
0
20
40
60
J J A S O N DJ F M A M J J A S O N
80 0
20
40
60
J J A S O N DJ F M A M J J A S O N
80 0
20
40
60
80
week in garden
Figure 6. Leaf size over time for coastal and inland garden plants by species. Generally 30 sibling plants from each of the study species were planted in a coastal
and an inland garden. Every two months from June 2006 to June 2007 and in November 2007 number of leaves, longest leaf length, and other data were
collected. Leaf linear size is the product of longest leaf length and leaf number. The gap between the coastal and inland lines represents the difference in size
between the plants growing in the two gardens. Note: D. b. blochmaniae and D. a. parva are summer-deciduous species so leaf data were available only part of
the year or for only a few individuals.
33
A 3.5
Sqrt(rosette weights + 0.5, g)
coast
inland
3
2.5
2
1.5
1
0.5
parv
n=30
n=24
P=1
% Reproductive
B
veri
25
23
.086
marc
26
21
ovat
26
19
agou
30
29
1
LANC CAES PULV
29
30
27 coastal
29
30
25 inland
1
.215
.447
veri
25
23
marc
26
23
ovat agou LANC CAES
26
29
30
30
21
29
30
29
.730
.601
1
100
80
60
40
coastal
20
inland
0
bloc
n=18
n=21
parv
30
26
PULV
27 coastal
25 inland
Figure 7. Comparisons of Dudleya species grown at coastal and inland gardens. Sibling plants of each
species were grown in a coastal and inland garden from June of 2006 to November of 2007. A. Rosettes
were collected and dried. Standard error bars are shown. B. Percents of reproductive individuals - number
of individuals reproductive spring of 2007 divided by total number of individuals for each species. Fisher’s
exact test probabilities are shown.
34
species except D. p. pulverulenta.
Reproduction – There were no significant differences between gardens for any of
the species (Figure 7B). Nevertheless, the rare species tended to have a greater number of
individuals reproduce in the coastal versus the inland garden (except D. b. blochmaniae
which had more individuals with inflorescences in the inland garden and D. c. agourensis
which had an equal proportion reproduce in both gardens). Common species showed the
opposite trend with a greater proportion of individuals producing inflorescences in the
inland garden than in the coastal garden, except D. p. pulverulenta, which had no
individuals reproduce in either garden. All species had earlier inflorescence production in
the coastal garden than in the inland garden (Appendix D Figure D-2).
Differential Environmental Responses – The two gardens provide additional
evidence for the limitation of the rare species’ ranges due to habitat characteristics. Seven
individuals died after surviving transplantation (alive in August 2006 but later dead), and
all were at the inland garden (4 ovat, 1 marc, and 2 parv; not including bloc). Considering
vegetative size, there was a strong negative correlation when the total biomass dry
weights of plants grown in the brick wall were plotted against the maximum difference in
size between the plants grown in the coastal and inland gardens (r = -0.962, P < 0.001, n
= 8: Figure 8A). Rare species (small biomass dry weights) had greater differences in size
than common species (large biomass dry weights). There was also a strong negative
correlation when total biomass dry weights of plants grown in a brick wall were plotted
against the difference in the proportions of reproductive individuals in the coastal minus
inland gardens (r = -0.910, P < 0.002, n = 8: Figure 8B). Rare plants had a greater or
equal proportion of reproductive individuals in the coastal garden than the inland one. In
35
contrast, two of the three common species (D. lanceolata and D. caespitosa) had
proportionally more reproductive individuals in the inland garden than in the coastal
garden. The other common species (D. p. pulverulenta) was not reproductive in either
garden.
A
B
1.3
0.2
parv
1.2
parv
1
% reproductive (Coast - Inland)
max size (Costal - Inland)
1.1
0.15
ovat
0.9
marc
0.8
veri
0.7
agou
0.6
LANC
0.5
0.4
0.3
-0.75
PULV
CAES
r = - 0.962, P < 0.001
-0.25
0.25
0.75
1.25
marc
0.1
0.05
ovat
agou
PULV
0
veri
LANC
-0.05
CAES
-0.1
r = - 0.910, P < 0.002
-0.15
-0.75
-0.25
0.25
0.75
1.25
log (Dry weight)
log (Dry weight)
Figure 8. Differential environmental responses. Sibling plants of each species were grown in a coastal and
inland garden from June of 2006 to November of 2007. Other siblings were grown in a brick wall garden.
These plants were grown between bricks in a thin layer of soil. Roots and rosettes
were collected and dried. Dry weights of the roots and rosettes of the brick wall plants were added for a
total biomass dry weight. A. The sizes of plants were measured by the log of the product of the longest leaf
length and number of leaves + 1. The difference in size was calculated between plants of each species in
each garden by subtracting inland garden size from coastal garden size. The maximum difference in size for
each species was then found. B. The percent of individuals reproductive spring of 2007 was divided by the
total number of plants in each garden for each species. The percent reproductive in the inland garden was
subtracted from that of the coastal garden for each species. Note: D. p. pulverulenta is in gray because none
of the plants were reproductive in either garden.
36
Discussion
The distributions of rare and common species in the Santa Monica Mountains area
reflect important life-history tradeoffs. With regard to reproduction and growth rare
species are at one end of the tradeoff, allocating energy to reproduction while seemingly
foregoing additional growth early in life. Common species are at the other end of the
spectrum, allocating energy to growth and foregoing reproduction early in life. The
outcome of this difference is that the rare species tended to be smaller in body size,
whereas the common species were larger in body size. This tradeoff between growth and
the amount of time it takes to reach reproductive maturity, in turn, had several effects.
First, the reproductive outputs of the larger, and more common, species were greater
(more fruits and seeds per fruit) than for the smaller, and rarer, species. Similar results
were found in a study by Lavergne et al. (2004). Secondly, the common species tended to
have larger seeds than the rare species which affected seedling survival, because the
larger the seed, the better the chance of seedling survival (Morin and Chuine 2006,
Mojonnier 1998). A third consequence, as seen in the comparison of coastal and inland
gardens, was greater adult survival under stressful conditions for the common species
(Appendix D). A fourth consequence of the tradeoff between body size and reproduction
is that the large common species had taller inflorescences in the field than the small rare
species, which would be expected to increase the distance that seeds disperse (Lloyd et al.
2003).
Another factor that can influence a species’ prevalence is specialization to
habitats that are found in low numbers or over a small geographic area. The rare species
occur in unique terrains (for example, serpentine and volcanic soils and rock outcrops),
37
while the common species have more generalized habitat associations. This is in keeping
with Gaston’s (1994) assertion that the sets of environmental conditions necessary for
rare species exist less frequently than those for common species. Within habitats,
conditions such as co-occurring vegetation, soil types, and climate can influence species’
distributions. The rare species seem to require the absence of other vascular plants and
the presence of mosses, lichens, or Selaginella, more specific soil types, aspects that are
closer to north facing, and climates that are cooler and more humid compared to the
common species. Although beyond the scope of the results reported here, the
morphological adaptations of the study species to their environment (having waxy leaves
in the form of a basal rosette and low allocation of energy to roots) also appear to be tied
to where they can live and, therefore, their distributions (Appendix A). The life-history
characteristics of the rare and common species differ in such a way as to affect their
geographic ranges and persistence in time (McKinney 1997, Brown et al. 1996). The
tradeoff between reproduction and growth has apparently led to the rare species having
smaller ranges and shorter expected times to extinction when compared with the common
species.
Life-history tradeoffs
Tradeoffs can occur between pairs of life-history traits (Stearns 1992). In the
current study, measured life-history traits were correlated in order to determine which
were involved in a tradeoff. Those traits involved in or affected by tradeoffs will be
discussed: size and age of first reproduction, number of seeds, size of seeds, and survival.
There is a tradeoff between size and age of first reproduction and number of seeds
38
(reproductive output) but not between the size of seeds and survival. Differences between
the rare and common species in size at first reproduction affect the other traits
contributing to the smaller distributions of the rare species when compared to the
common ones.
The tradeoff between growth and reproduction is also reflected by relationships
between size at maturity and number of offspring. Sterns (1992) reviewed the advantages
and disadvantages of early versus delayed reproduction. The advantages of early
maturation are a greater probability of surviving to maturity and higher fitness because
offspring are produced early in life and those offspring reproduce earlier but at the
possible cost of higher mortality rates of offspring than if reproduction were delayed.
Theory generally suggests that there is strong selection for early maturity in the absence
of tradeoffs. However, reproduction will be delayed if it results in greater lifetime
reproductive success and there will be a tradeoff between this increase and lost fitness
associated with longer generation times and lower survival to maturity. For example, if
delayed maturity permits further growth, and if fecundity increases with size, then a
benefit of delayed maturity would be higher eventual fecundity than would be attained if
maturity were reached at a smaller size (Stearns 1992). This is the case comparing the
Dudleya species in the Santa Monica Mountains area. For example, the small rare D. c.
marcescens produced on average 10 fruits and 44 seeds per fruit. In contrast, the huge
common D. p. pulverulenta produced on average 167 fruits and 551 seeds per fruit.
Lavergne et al. (2004) found that rare species in many genera produce fewer seeds than
congeneric common species. Not only does lower seed production negatively affect not
39
rates of population persistence, it limits opportunities for colonization of new habitats,
which might also affect species’ distributions (Lavergne et al. 2004).
Another tradeoff is between the number of seeds produced and the size of the
seeds. This is a tradeoff between seed size and the likelihood of seed survival and
seedling establishment. Plants can produce either a small number of large well
provisioned seeds that are each likely to germinate and become established, or they can
produce many small low quality seeds that, individually may (or may not) be successful,
but are so numerous that they have a high combined chance of establishment (Gurevitch
et al. 2006). For the Dudleya species evaluated for this study, the rare species tended to
have smaller seeds than the common species (except for D. p. pulverulenta), and these
seed size differences translated into differences in seed germination and seedling
survival. As seed size increased, so did seed germination and seedling survival. For
instance, the rare D. c. ovatifolia had seed projected areas averaging 0.254 mm2, 59%
germination, and 40% seedling survival compared to the common D. lanceolata with
seed projected areas averaging 0.369 mm2, 80% germination, and 75% seedling survival.
Other studies have also found positive relationships between seed size and the probability
of germination and establishment (Morin and Chuine 2006, Mojonnier 1998 and citations
therein). These traits were not found to be involved in a tradeoff, but differences between
species could contribute to differences in prevalence.
The number of individuals that survive in each species can affect the chances of
that species persisting, with high survival increasing the probability of persistence. When
rare and common species are compared, the greater reproductive outputs and higher rates
of seedling establishment for common species improves the likelihood of their population
40
size being augmented and reduces the chance of genetic diversity eroding. Large patch
size can also increase the probability of dispersal of seeds of the common species to other
suitable areas (Lavergne et al. 2004, Karron 1997, Gaston 1994), enabling common
species to be more widespread. Morin and Chuine (2006) also found that life-history
traits can affect species’ ranges. Specifically, those tree species with earlier reproduction,
shorter heights, and lower seed mass had smaller ranges.
Environmental dependence of species’ prevalences
A species will increase its range until it no longer finds the environmental
conditions it needs (Levin 2000). Conditions that can impede a species’ spread include
the presence of other organisms as well as adverse soil and climate conditions
(Kruckenberg and Rabinowitz 1985, Stebbins 1978). If habitats with the conditions
necessary for the persistence of a species are uncommon or of limited size, then the
distribution of species that occupy them will necessarily be low as well (Gaston 1994,
Burgman 1989, Kruckeberg and Rabinowitz 1985).
One element that can affect the distribution of species involves competition from
(Ackerly 2003) or facilitation with (Kruckeberg and Rabinowitz 1985) various other
organisms. There were differences between the rare and common Dudleya species in cooccurring vegetation. Rare species were associated mostly with mosses, lichens, and
Selaginella, low stature plants, whereas the common species were often found in close
proximity to taller plants. The ability of common species to co-occur with a wider range
of plant growth forms may be because of their superior competitive abilities and
tolerances associated with being of larger size and having a greater reproductive output
41
compared to the rare species (Gurevitch et al. 2006). A study by Lavergne et al. (2004) of
congeneric pairs of narrow endemic and widespread species, also found that narrow
endemics occurred in vegetation with a lower canopy and a smaller number of coexisting
species, indicating reduced competitive abilities when compared to widespread
congeners. The negative effects of competition – reduced growth, reproduction, and
survival (Gurevitch et al. 2006) – may preclude rare species from existing in habitats with
other vascular plants, thereby limiting the habitats in which they can persist.
Riefner et al. (2003) and Riefner and Bowler (1995) have presented evidence that
the presence of biological crusts, lichens, mosses, and/or Selaginella may facilitate
seedling recruitment of the rare Dudleya species studied herein. Biological crusts fix
nitrogen and thereby increase soil fertility, stabilize soil surfaces, improve percolation
and soil moisture storage, and reduce erosion. Lichens collect nutrient-rich fog
condensation, soil particles and moisture, and may provide protection from herbivory and
decrease establishment of other vascular plants. Mosses and Selaginella collect moisture
and soil. All of them produce sites for establishment on rocks that would not be present
otherwise increasing space for seedlings to recruit and the chances of successful
establishment to a larger size. Dependence on the presence of bryophytes in order to
persist in a habitat may limit the abundance of those species with this requirement
Riefner et al. (2003).
Another feature of a habitat that can affect species’ distributions is soil type. Each
of the Dudleya listed as threatened occurs in a different habitat with unique geological
substrates that apparently limit its distribution. Dudleya a. parva is found on Conejo
volcanics, D.verityi exists on volcanic rock outcrops, D. c. marcescens occurs on sheer
42
volcanic rock surfaces, D. c. ovatifolia grows on sedimentary conglomerate rock
formations, and D. c. agourensis lives on dissected gravels from the late Pleistocene
(USFWS 1999). Dudleya b. blochmaniae, the species of intermediate rarity, occurs in
clay or serpentine soils that are rocky (Bartel in Hickman 1993). In contrast, the common
species are found in rocky or coastal habitats in which rock/soil types vary. Dudleya
lanceolata grows on rocky slopes, D. caespitosa lives coastally, and D. p. pulverulenta
grows in a variety of rocky places (Bartel 1993). The rare species are adapted to
geological formations that have smaller and more fragmented distributions than the
common species.
A third environmental factor that may play a role in species’ distributions is
climate. All of the study species use the CAM photosynthesis pathway and therefore are
limited to regions with regular seasonal rains (Luttge 2004). Also, Dudleya may, to
varying degrees, require the cool humid climate available along the coast as evidenced by
their mostly coastal distribution (Ulh 2004, 1994). Within the broad category of
mediterranean-type climates, there can be levels of humidity and temperature to which
the species may react differently. The rare versus common species’ performance in the
mesic coastal and xeric inland gardens provide evidence for differences in physiological
tolerances to stressful conditions. The rare species had smaller linear leaf sizes, rosette
dry weights, a smaller proportion of individuals reproduce, and poorer survival in the
inland garden compared to the coastal garden. For example, the linear leaf sizes for D. c.
ovatifolia in April (when they would be reproductive) were1.943 in the coastal garden
versus 1.289 in the inland garden. Broken down into its components, longest leaf lengths
were 5.6 versus 2.55 and leaf numbers 16.69 versus 11 in the coastal versus inland
43
gardens, respectively. For rosette dry weights, D. verityi had the greatest difference in
weight between gardens (1.400 g inland and 1.932 g coastal). With regard to reproduction
D. a. parva had 81% reproduction in the inland garden and 97% in the coastal garden.
Finally, of the few deaths attributable to climatic conditions, more occurred in the inland
than coastal garden and all were of rare species. The inability of a species to survive and
reproduce in a habitat keeps it from expanding throughout that habitat (Brown et al. 199).
The decreased size of the rare Dudleya species in the inland compared to the coastal
garden may be attributed not only to their poorer survivorship, it likely had a negative
effect on reproduction. Though the decrease in the proportion of individuals that were
reproductive in the inland compared to the coastal garden was not significant, the smaller
size of plants in the inland garden plants likely led to smaller reproductive outputs
compared to plants in the coastal garden. Combined these results suggest the rare species
would not persist under dry hot conditions and, therefore, were limited in the habitats
available for them to occupy. The common species, on the other hand, had smaller
differences in linear leaf sizes and tended to have a greater proportion of individuals
reproduce in the inland garden compared to the coastal garden suggesting they were less
limited in the habitats they could occupy than the rare species.
Conclusion
The life-history tradeoff between growth and reproduction in rare and common
Dudleya species has a macroevolutionary impact. As a result of this tradeoff the rare
species have small body sizes engendering poorer abilities to reproduce, compete with
other plants, and tolerate hot dry conditions than the larger bodied common species.
44
These limited abilities appears to be part of their specialization to very specific
environmental conditions, where they could be successful by avoiding competition
(Lavergne et al. 2004), but at the cost of their abilities to adapt to new habitats when the
opportunity for colonization became available (Kunin and Gaston 1997). The common
species, with their larger body size, have superior reproductive and competitive abilities
and physiological tolerances to hot dry conditions as evidenced by their abilities to
coexist with a broader range of vascular plants and perform better in the stressful xeric
inland garden than the rare species. A consequence of the common species’ larger body
sizes was their ability to become generalists, persisting in a wide variety of habitat
conditions, relative to the rare species. Thus, the common species were better able to
adapt to new habitats when colonization opportunities arose. The narrow habitat
requirements of the rare species resulted in there being few suitable habitats for them to
occupy making them more prone to extinction than the generalist common species with
broad habitat requirements and geographic ranges (McKinney 1997). The selection
processes that lead to the adaptation of the species to their habitats probably occurred at
the level of individuals. The differences in life-history traits resulting from the tradeoff
and its effect on other traits may have set the stage for later higher-level selection at the
species level. The greater extinction probability of the rare species as compared to the
common species in conjunction with their current distributions exemplifies how lowerlevel selection processes can shape higher-level ones (Gould 2002). To say, though, that
rarity in some Dudleya species is because of life-history tradeoffs and dependence on
habitat conditions would be an oversimplification. This study focused on only a few of
the time scales, ecological processes, and factors that could have affected the
45
distributions of Dudleya species of the Santa Monica Mountains area. Also, the
generalizations put forth in this thesis do not hold true for every Dudleya species. For
example, D. p. pulverulenta, a common species, is one of the largest in body size and yet
produces the smallest seeds. Exceptions are not limited to common species nor to lifehistory traits. Microhabitat requirements for the rare species are not all the same. Dudleya
c. marcescens and D. c. ovatifolia have a habitat requirement for shade that is not found
in the other species. In conclusion, there is more than one reason for rarity and when one
reason is given for multiple species there will be exceptions.
46
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49
Appendix A: Interpretative background on Dudleya
The thesis is best understood if one has contemplated the natural history of
Dudleya in general and more particularly the nine species that were studied. Morphology,
physiology, phenology, and details of the geographic range come together in a
speculative interpretation of adaptations, and the interpretation suggests hypotheses that
could, in principle, be tested. Much of this interpretation, however, was done after, not
before, the project was set up; thus, the following discussion may be useful in setting up
additional studies, as well as pondering the implications of the current one.
Dudleya is a genus of perennial succulents in the family Crassulaceae, the
Stonecrop Family (Bartel in Hickman 1993), that uses the crassulacean acid metabolism
(CAM) photosynthetic pathway (reviewed by Dorsey 2007). Dudleya grow on rock
outcrops in cracks, on saxicolous mosses or lichens, with Selaginella, or in shallow soil
deposits on rocks and nutrient-poor mineral soils often surrounded by grasses (Riefner et
al. 2003, Riefner and Bowler 1995, pers. obs.). The growing season of Dudleya starts
with winter rains and extends through the spring. Inflorescences can start to form as early
as December. Some species bloom as early as March, others as late as July. They stay in
bloom for two to three months (McAuley 1996). Over the summer, Dudleya become
physically dormant: inflorescences dry out and may break off, the leaves of the rosette
close, and the outermost leaves become dry but in most species remain intact. Dudleya a.
parva and D. b. blochmaniae have leaves that are summer deciduous. The fruits ripen
over the summer. Seeds are dispersed starting in late summer when the follicles become
dry and open. Most seeds fall close to the parent plant (Marchant et al. 1998), but some
are dispersed by the wind. Seed germination is activated by rain (or persistent moisture).
50
After consistent rains, the rosettes open revealing the living inner leaves, and growth
resumes. For the species with summer deciduous leaves, new growth is from a corm (D.
b. blochmaniae) or caudex (D. a. parva).
The above and below ground morphologies of Dudleya species enable them to
live in dry rocky habitats. A basal rosette allows for the maximization of leaf area for
photosynthesis. Because leaves are basal, little energy needs to be put into developing a
supporting stem and its low stature protects the plant from wind and other mechanical
damage (Stebbins 1984). The rosette habit of Dudleya species may allow them to take
advantage of small amounts of available moisture in the form of fog. Water from the fog
collects on the leaves and is channeled to the roots by flowing down the stem. This ability
is even greater when plants have a waxy epidermis, such as agaves, that can channel as
little as 1 mm of rain (Martorell and Ezcurra 2002). Dudleya are likely to be able to do
this as well, as indicated by their ability to grow roots in response to high levels of
humidity (Riefner et al. 2003). Of the study species, all but three (D. b. blochmaniae, D.
c. marcescens, and D. c. ovatifolia) have glaucous leaves (Bartel 1993, Nakai 1987,
Moran 1951). Having wax on the leaves may not be important for D. b. blochmaniae and
D. c. marcescens because their leaves are not living during the hot dry summer (Moran
1951, pers. obs.) and for D. c. ovatifolia because they occur where it is shaded (USFWS
1999; Figure 4). This ability to take advantage of small amounts of condensation may
help Dudleya endure the long summer drought, but it may limit the species that need this
source of water to coastal or shaded inland habitats (where D. c. marcescens and D. c.
ovatifolia occur; USFWS 1999) as evidenced by the rare species’ reduced size,
51
reproduction, and survival when in a drier hotter inland environment than when in a
cooler moister coastal one.
An additional adaptive feature related to water stress is the ability of rosetteforming species to let their outer leaves dry and transfer the water and nutrients to the
inner leaves (Luttge 2004, Mulroy 1979). Being able to retain leaves year round allows
plants to maximize rainfall by being able to store water and resume active photosynthesis
quickly as opposed to having to grow new leaves first (Ting and Rayder 1982, Mulroy
1979). This is especially important when timing and amount of rainfall varies from year
to year. There can be other advantages to only retaining below-ground structures. Those
species with leaves living only part of the year (D. b. blochmaniae, D. a. parva, and D. c.
marcescens) are able to escape from the problems of aging because new parts are grown
each year, and from harsh conditions, so energy does not have to be put into adaptations
to those conditions which might decrease physiological performance (Pugliese and
Kozlowski 1990).
The environment in which a plant occurs can also influence its below ground
morphology. The study species have thick branched main roots and fine lateral roots
(pers. obs.), a morphology ideal for dry rocky habitats. The thick part of the roots can be
used for storage to help the plant withstand the long summer drought. The branching can
facilitate growth around rocks or in different directions in order to cover more completely
the surrounding available area than if the roots did not branch. The fine roots allow for
growth in narrow spaces between the rocks or in cracks. Energy allocation to roots in the
study species (Figure C-3) may be low relative to many other kind of plants. Root growth
in Dudleya saxosa (Nobel and Zutta 2007) and desert succulents (Nobel et al.1989) has
52
been found to be optimized to only the volume of soil that would be necessary to absorb
enough water to fill the storage capacity of the plant. Root growth may be limited by the
rockiness of the soil as well. In a study of Agave deserti, a slow growing CAM succulent,
Martre et al. (2002) showed that as the rockiness of the soil increased the volume of roots
decreased.
53
Appendix B: Nested ANOVAs and correlations
In the Results, significance tests are presented as to whether or not there was
variation among species for a given feature, and whether or not there was an added
difference between the three common species and the five (to six) rare species. Table B-1
presents the nested ANOVAs in more detail.
Later in the Results, some correlations were presented between one trait and
another, with n equal to 8 or 9 species (Figure 3). Table B-2 presents the means of the
traits by species. Table B-3 presents the correlations among traits in a more exhaustive
manner than in Figure 3.
Table B-1. Nested ANOVAs. For various traits, individuals at 2-3 sites were pooled for each “species,”
species-within-rarity was tested over the error, and rarity was tested over species-within-rarity (the latter
being a weak test because there were only 3 common species and 5 rare species).
Trait
error MS
(df)
20519
(261)
633
(261)
1316
(261)
0.036
(203)
0.359
(203)
0.020
(261)
0.616
(261)
0.004
(254)
0.00096
(87)
0.096
(514)
0.055
(514)
Average distance to nearest neighbors, cm
Microsite slope, degrees
Degrees from due north
Log(Leaf length, cm)
Sqrt(Leaf number)
Log(Inflorescence height, cm)
Cubed root(Number of fruits)
(Seeds per fruit) - 1/6
Seed projected surface area, mm
Arcsine(%Germination)
% Survival
NS P>0.1; †P<0.1; *P<0.05; **P<0.01; ***P<0.001
54
spp ⊂ rarity MS
(7 df)
767358***
rarity MS
(1 df)
889790 NS
12772**
823.869 NS
36918**
27449 NS
1.056**
18.162**
54.238***
157.853 NS
0.641***
30.023***
13.196**
176.843**
0.107***
0.779*
0.01636**
0.20778**
1.044*
1.627 NS
1.167**
1.446 NS
Table B-2. Means of selected traits for each species. See Figures 3 and 4 with associated text for explanation of traits.
# fruits (1/3)
seeds per fruit –(1.6)
seed projected area
arcsine germination
% seedling survival
log inflorescence height
nearest neighbors distance
degrees from north
slope
log (root+shoot) in brick wall
log(root/shoot)
reproduction out of 3 springs
log reproductive output in the wild
bloc
2.429
-0.633
0.298
0.851
60.610
1.009
7.598
98.000
23.733
-
parv
2.743
-0.562
0.330
0.932
70.520
1.110
10.775
20.000
24.000
-0.499
-0.247
2.898
2.936
veri
3.222
-0.574
0.247
0.668
47.070
1.060
6.255
37.333
39.100
0.321
-0.474
2.825
3.142
marc
2.093
-0.570
0.246
0.559
29.720
0.987
6.630
13.000
69.600
0.056
-0.444
2.792
2.615
ovat
2.539
-0.523
0.254
0.647
39.980
1.022
25.786
20.333
66.500
0.086
-0.597
2.534
2.998
agor
4.037
-0.522
0.288
0.715
55.770
1.390
68.256
100.000
57.167
0.337
-0.409
2.454
3.659
LANC
4.253
-0.455
0.369
0.966
75.290
1.813
168.001
44.667
30.833
0.579
-0.287
1.828
4.033
CAES
4.200
-0.538
0.427
0.855
66.740
1.663
50.815
22.167
72.000
1.046
-0.415
0.621
3.679
PULV
5.230
-0.351
0.185
0.720
43.550
1.934
501.399
13.333
48.333
0.868
-0.895
0.026
4.964
Table B-3. Correlations between traits, calculated across 9 species, except those involving the last four variables which were calculated across 8 species (without
D. b. blochmaniae).
–(1.6)
seeds per fruit
seed projected area
arcsine germination
% seedling survival
log inflorescence height
nearest neighbors distance
degrees from north
slope
log (root+shoot) in brick wall
log(root/shoot)
reproduction out of 3 springs
log reproductive output in the wild
# fuits (1/3)
0.820
seeds per fruit –(1.6)
0.073
-0.271 seed projected area
0.275
0.036
0.713
arcsine germination
0.293
-0.041
0.793
0.968
% seedling survival
0.946
0.835
0.210
0.394
0.368
log inflorescence height
0.793
0.925
-0.390
0.040
-0.078
0.790
nearest neighbors distance
-0.039
-0.362
0.111
0.190
0.297
-0.137
-0.240 degrees from north
0.047
0.125
-0.045
-0.633
-0.558
0.048
-0.027
-0.339 slope
0.787
0.551
0.182
0.078
0.096
0.783
0.543
0.042
0.354
log(r+s)
-0.404
-0.664
0.714
0.512
0.610
-0.301
-0.731
0.296
-0.327
-0.437
-0.834
-0.767
-0.083
-0.224
-0.140
-0.869
-0.787
0.231
-0.202
-0.846
0.966
0.924
-0.092
0.304
0.238
0.934
0.914
0.105
-0.152
0.730
55
log(r/s)
0.584
-0.551
repro3
-0.852
Appendix C: The brick wall garden
The brick wall garden consisted of plants grown between clay bricks with a thin
layer of soil. A 10 × 4’ wooden structure with 3’ perpendicular sides made of 1/2”
plywood and 2 × 4s set at an angle was used as a support structure for the bricks to rest
against. The wooden backing was supported by 2 × 4s the ends of which were cut at an
angle so they were flush with the plywood and the ground. To increase the support from
the ground, the area where the 2 × 4s rested was dug up and a brick was put under each 2
× 4. Pieces of rebar were pounded into the ground behind the plywood and between the 2
× 4s to give added support to the plywood. Concrete bricks were placed along the back
side of the plywood at ground level to keep the base in place. Four by fours were placed
in front of the structure. One end of the bottom row of bricks was placed on the 4 × 4 and
the other on the ground so the back side of the brick was flush against the wooden
support. Bricks were laid lengthwise, perpendicular to the support structure. An 8” × 4’
piece of hardboard was vertically placed between each brick column. As each brick was
laid a 1/4 inch thick layer of one part potting mix used with the potted plants and one part
potting soil was placed on it. A randomly chosen individual of a pre-chosen species was
placed in the soil, a drip irrigation hose was placed over the plant, secured with wire to
the hardboard, and another brick was put on top. This was repeated until one row of
plants was in place. The next row of bricks was constructed the same way. The species
were arranged such that from column to column the order of the species from top to
bottom was shifted by one. This allowed for variation in the location of a given species’
individuals both left to right across rows and up and down across columns. There were 9
rows and 28 columns total. The garden was constructed from 7 – 17 July 2006. The
56
brick-wall garden was north-facing on the California State University, Northridge
campus (34.239o N, 118.531o W). The campus is in the hot dry valley well inland of sites
that elsewhere are referred to as “inland.”
Figure C-1. Photo of brick wall garden shortly after planting.
Plants were watered every 4 to 5 days for a total of 4 times after transplantation.
Watering was resumed 11 November 2006 to 12 July 2007, weekly. From July 2006 to
September 2007, every two months, data on the number of leaves, longest leaf length,
and number of inflorescences of each individual were logged. Buds and flowers were cut
from the inflorescences as necessary to limit the amount of energy allocated to
reproduction (Jongejans et al. 2006) and control for energy allocation differences
between reproductive and non-reproductive individuals.
Plants grown in the brick-wall garden were intended to approximate more natural
growing conditions than plants grown in a pot. In all of the species, sizes (as measured by
longest leaf length multiplied by leaf number) decreased in late summer and fall, when
plants started to show signs of physical dormancy, and increased in winter and spring,
during the growing season (Figure C-2). The common species tended to be larger in size
than the rare ones. The exceptions being D.verityi (rare) and D. lanceolata (common)
57
Between subjects
Species
Error
df
7
204
MS
29.535
0.629
F
46.968***
Within subjects
Date
Date × Species
Error
***P<0.001.
7
49
1428
11.308
0.374
0.04253
265.851***
8.786***
3
2.5
CAES
log(linear size + 1)
PULV
2
veri
LANC
1.5
agou
ovat
marc
1
parv
bloc
0.5
0
0
10
20
30
40
50
60
Week in brick wall
Figure C-2. Changes in size of plants over time. Size measured as the log(longest leaf length × number of
leaves + 1). Week 0 was 17 July 2006. Inset repeated measures ANOVA done without bloc.
both of which were very close in size, with one being larger than the other or visa versa
over time. Dudleya lanceolata tended to have longer leaves than D. verityi, but D. verityi,
a clonal species that forms multiple rosettes, tended to have more leaves than D.
lanceolata.
From September 2007 to November 2007, plants were removed from the brick
wall garden. At the time of removal the wire attaching the irrigation drip hose was
removed, the brick above the plant was removed, the drip hose was moved out of the
58
way, the brick the plant was resting on was lifted taking care not to break any roots,
pressure was applied to the soil mass from the sides, and the rosette was lifted up. Once
the soil was loose, the plant and intact roots were removed. The rosette was cut from the
roots below the leaves (at the root crown). All of the dried inflorescences were removed
from the rosette, and an ink imprint was taken of the cross-section. Rosettes were placed
in labeled paper bags. The roots were held up near the cut to allow loose dirt to fall away
and were then placed in a bucket two-thirds full of water. As much soil as possible was
removed from the roots by flexing the roots slightly, separating roots from each other,
and gently rubbing the soil off the roots. The roots were then placed in another bucket
that was half filled with water. The roots were gently swirled in the water and the above
process was repeated to remove as much remaining soil as possible. The very finest roots
were lost in this process as they disintegrated when the soil was removed. Remaining
larger pieces, such as perlite and peat were picked or pushed out of the roots, using a
dissection-kit needle probe. The roots were then laid on a brick and allowed to dry before
being placed in a labeled paper bag. A strainer was used to remove as much soil from the
first bucket as possible after each plant. When the water became dirty it was replaced. At
this time the second bucket became the first and visa versa. After a whole column was
completed, the wires were removed from the drip irrigation hose and the now exposed
hardboard. The hardboard was removed to gain access to the next column of bricks.
These steps were repeated until all of the plants had been removed. Bagged roots and
rosettes were placed in plastic full-sized flats. The flats were put in a drier set at 37.8o C
until weights stopped decreasing, which took months of drying.
59
14
Dry weight (g)
12
Rosette
Root
10
8
6
4
2
0
parv
ovat marc agou veri LANC PULV CAES
Figure C-3. Root and shoot dry weights. Plants of each species were grown in a thin layer of soil between
vertically stacked bricks from July 2006 until November 2007. When the garden was dismantled roots were
separated from rosettes and cleaned. Roots and rosettes were dried until weights started to increase. Sample
sizes n = 21 to 29.
60
Appendix D: More information on coastal versus inland gardens
In the Results comparing coastal and inland gardens, data were presented on how
leaf size changed through the seasons, final rosette weight, and the percentage of plants
that bolted. Corresponding ANOVA tables are here presented along with data on root
crown cross-sectional surface areas, which is another measure of size. When plants were
harvested, they were cut at the base of the rosette. An ink print was taken of the crosssection. From the ink prints of the root crowns, the longest diameter and the one
perpendicular to it were measured using a ruler. The cross-sectional area of the roots
were calculated using the formula for the surface area of an ellipse (SA = πr1r2). In the
case of multiple rosettes or root branching, measurements were taken of each crosssectional area and areas were added. The largest cross-sectional surface area was
measured for the common species, D. caespitosa, and the smallest for the rare species, D.
a. parva. Dudleya caespitosa is one of the largest study species and has the ability to
produce multiple rosettes. Dudleya a. parva, is one of the smallest study species with
living leaves present only part of the year.
Table D-1. Repeated measures ANOVA of log([maximum leaf length × number of leaves] + 1)
between individuals
rarity
garden
rarity × garden
spp ⊂ rarity
garden × spp ⊂ rarity
error
df
1
1
1
6
6
426
MS
158.6166
159.3713
16.90972
33.84762
1.49176
0.56536
F
4.686
106.834
11.335
no test
no test
P
0.074
<0.001
0.015
within individuals
date
date × rarity
date × spp ⊂ rarity
date × garden
date × rarity × garden
date × garden × spp ⊂ rarity
error
7
7
42
7
7
42
2982
13.904
1.31737
0.43258
3.57332
0.54368
0.22784
0.03275
3.21E+01
3.045
no test
15.683
2.386
no test
<0.001
0.011
61
<0.001
0.038
Table D-2. Split-plot ANOVA of square root(rosette weight). Effects of coastal versus inland garden, rarity
class, and species within rarity class. Total n = 423. R2 = 0.692.
df
1
6
1
1
6
407
rarity
species ⊂ rarity
garden
garden × rarity
t×s⊂r
error
MS
130.76297
6.58217
15.93847
1.30727
0.63795
0.21054
F
19.86624
31.26378
24.98389
2.04917
3.03011
P
0.004
<0.001
0.002
0.202
0.007
Table D-3. Split-plot ANOVA of log(root crown cross-sectional area + 1). Effects of coastal versus inland
garden, rarity class, and species within rarity class. Interaction terms dropped sequentially when P > 0.25.
Total n = 423. R2 = 0.592.
df
1
6
1
414
rarity
spp ⊂ rarity
garden
error
MS
10.82183
3.30078
0.39659
0.05306
F
3.279
62.205
7.474
P
0.120
<0.001
0.007
0.45
coastal
log(cross sectional area + 1)
0.4
inland
0.35
0.3
0.25
0.2
0.15
0.1
0.05
parv
veri
marc
ovat
agou
LANC CAES PULV
Figure D-1. Coastal and inland root-crown size by species. Sibling plants were grown in a coastal and an
inland garden from June 2006 to late November (inland) or mid-December (coastal). When the plants were
removed the rosettes were collected and ink imprints of the root-crown were taken. Standard error bars are
shown. For sample sizes, see Figure 7A.
62
Proportion bolting
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
veri
parv
bloc
agou
marc
ovat
LANC
CAES
PULV
coastal
inland
0
20
40
60
80 0
20
40
60
80 0
20
week in garden
Figure D-2. Bolting through the seasons in the coastal and inland gardens. See Figure 6 for timeline.
63
40
60
80
Appendix E: Watering treatments
When the thesis project was being set up, there was a large portion of the research
that was devoted to trying to find physiological differences between the species and how
they might depend on air temperature and humidity and soil moisture. In order to
determine if stressful habitat conditions could affect the physiological performance of the
study species, three sets of plants were subjected to three watering treatments in an
experimental garden in which they were exposed to hot dry summers: a group with no
water added, a group that was misted, and a group that was watered weekly.
As transplantation of seedlings was being done, two 1 × 1” travertine tiles were
placed to either side of the seedling in these three treatments. The tiles were intended to
assure that there would be a space below the plant’s rosette for an infrared-gas-analyzer
chamber to be cuffed on, so photosynthesis readings could be taken. However, the plants
quickly grew too big for the chamber to be used, so gas exchange was never measured.
Photosynthetic activity was measured, more ambiguously, by light-adapted fluorescence,
which does not allow one to interpret whether plants are doing CAM photosynthesis or
regular C3 photosynthesis. There were more serious problems, though, with the wateringtreatments experiment, so limitations in the photosynthesis related variables turned out to
be a moot point.
The three sets of potted plants were kept on the California State University,
Northridge campus, where summers are as hot as the hottest areas in the Santa Monica
Mountains. The water group was watered weekly unless it rained, in which case they
received no additional water. The misted group was intended to be cooled by misting
without having water added to the soil. For the first 20 days, misting was controlled by a
64
timer capable of being set “on” or “off” only, so plants were misted constantly for a set
period of time; thereafter, the mist group was misted every 15 minutes for three or five
seconds. Misting was done during the 4 warmest hours of the day, from 12:00 noon to
4:00 p.m. May through October and 11:00 a.m. to 3:00 p.m. December through February.
The duration of the misting was longer June through November (5 seconds) and was
shorter December through May (3 seconds). The group was misted even if it rained. The
last group, the no-water group, received natural precipitation only, which meant basically
no water from June to November. The treatments were started in early June.
Each treatment group was kept in a separate bay. The three bays were constructed
under a large shade-cloth awning. The walls between the bays consisted of a 2 × 4 frame
over which additional shade cloth was secured. The walls were 6 feet high and 7 feet
long. The mister system was constructed from 2 × 2s in the form of a cube frame raised
to a height of 5 feet above the pots. The mister hose and nozzles were secured along the
frame. The frame was centered over the plants. The potted plants were kept in flats set on
wooden pallets. The flats in each treatment group were rotated weekly, and each group
was moved to a different bay monthly. It should be noted, however, that plants in a
treatment were kept next to one another, so there was spatial pseudoreplication in the
application of the treatments, although not in the assigning of seedlings to treatments.
One HOBO meter was placed in each treatment bay starting on 8 June 2006 to log
temperature, dew point, and humidity. The HOBO for each treatment group was moved
to follow the treatment group from bay to bay as the flats for their treatments were rotated
each month.
65
Every three months, the sizes of plants were determined by placing white pieces
of paper underneath the leaves, placing a ruler next to the plant, taking a photograph of
the plant with a camera on a tripod centered over the plant, and using NIH Image
software to find the projected area of the plant. Any dry inflorescences, buds, or flowers
were removed from the plant before taking the pictures so only photosynthetic plant parts
were included. Buds and flowers were removed in order to limit allocation of energy to
reproduction (Jongejans et al. 2006) and to control for energy allocation differences
between reproductive and non-reproductive individuals. Pictures were taken every three
months from May 2006 to July 2007. At the end of the experiment the projected surface
areas of all species in the three watering treatments in April 2007 were compared using
an ANOVA. Tukey pairwise comparisons were done to compare the projected surface
areas of each species grown in the three watering treatments.
Photosynthetic activity was determined by using a PAM fluorometer (PAM-2000,
Walz, Effeltrich, Germany; Cleavitt 2002). In order to minimize the effects of
temperature throughout the seasons, flats of pots were placed in a greenhouse for at least
2 1/2 hours before fluorometer readings were taken. On a few occasions, plants were left
in the greenhouse overnight. The readings were taken in the greenhouse. Temperature
and light level readings for the greenhouse were recorded hourly until two hours before
sunset when levels were recorded every 1/2 hour. Six readings were taken on each plant:
spots on the upper and middle part of an outer leaf, the upper and middle part of a middle
leaf, and the upper and middle part of an inner leaf. Data analyses were done using the
2nd from the maximum reading in order to show the highest potential yield while
eliminating possible outliers. Readings were of light-adapted effective quantum yield.
66
Readings were taken over three consecutive days, one treatment group at a time, every
two weeks, from August 2006 to January 2007, then monthly for the next two months.
Presence of inflorescences was also recorded.
Unfortunately, the three watering treatments experienced fairly similar
temperature and humidity regimes (Figure E-1); misting did not lower the temperature
nor did it raise the humidity in a way comparable to the difference between the coastal
and inland gardens. Nevertheless, comparing the temperature (Figure E-1A) in the hot
season, the no-water treatment temperature was hotter than the water and mist treatments,
which were often similar. In late October and parts of November, the mist treatment had
the highest temperatures followed by water and no-water, which were mostly similar.
From the end of December through February, temperatures in all three treatments were
mostly the same.
Comparing the humidity (Figure E-1B) from August through the end of
November, the water treatment had the lowest percent humidity. During this time period
the mist group had higher percent humidity than the no-water group with differences
being the greatest in August and early September. In December the percent humidity for
all treatments was essentially the same. January through March the mist and no-water
groups had similar percent humidity with the mist treatment often being slightly higher.
Periods of low humidity, as measured in the no-water group daily averages from 12:00 –
3:00 p.m., were from August through mid-September (below 30%), late October (below
30%), early to mid-November (20-30%), early December (below 20%), January (below
20%), and early March (below 20-30%).
67
A
mist
50
Temperature C
(averaged noon-3 pm)
water
no water
40
30
20
10
0
13
17
8
A
13
S
17
O
22
26
31
35
40
100
% Humidity
(averaged noon-3 pm)
B
8
80
60
40
20
0
22
26
31
35
40
N
D
J
F
M
Week of Treatment
Figure E-1. The average temperature (A) and percent humidity (B) of three watering treatment areas from
12:00 pm to 3:00 pm over time. HOBOs were placed in each of the three water treatment areas (mist,
water, and no water) and readings were taken every 15 minutes from June 2006 to July of 2007. Graphs
show data from August 2006 to March 2007 when photosynthesis readings were being taken. Sibling plants
from each species were randomly placed into each of the three treatments. Mist plants received misting for
3-5 seconds every 15 minutes from 11:00 am to 3:00 pm when temperatures were cool and from 12:00 pm
to 4:00 pm when temperatures were hot. Water plants received water once a week. No-water plants
received natural precipitation only. Figure B note: the humidity sensor in the water treatment HOBO
stopped working properly at the end of December.
68
C
45
Temperature C
35
temp max mist
25
temp min mist
temp max water
15
temp min water
temp max no water
5
temp min no water
-5
8
S
O
N
D
J
F
13
17
22
26
31
35
M
40
Week of Treatment
Figure E-1 continued. C. Temperature maximums and minimums for all water treatment groups with PAM
reading dates. Sibling plants were randomly placed in one of three watering treatments: water, mist, and
no-water from June 2006 through June of 2008. The water group received water or natural precipitation
once a week. The mist group was misted for the four warmest hours of the day and received natural
precipitation. The no-water group received natural precipitation only. HOBOs were placed in each of the
treatment areas from June 2006 through July of 2007 to measure temperature and percent humidity. The
gray bars show the dates when quantum effective yield readings were taken using a PAM fluorometer.
Although the treatments were similar, temperature strongly changed through the
seasons (Figure E-1C), so season × species interactions may be interesting. The highest
maximum daily temperatures were from August through mid-September ranging from 30
– 45 oC. There were also high temperatures (low 30s) for a few days in late October,
early and mid-November, and early March. In late December temperatures dropped to 0
and 1 oC for two consecutive evenings. Temperatures dropped again in mid-January to -4
C and three nights later to 1 oC. Even as late as the end of February there were three
nights where temperatures were 2 oC.
69
Rare species had plants with smaller projected areas than common species (Figure
E-2). Also, rare species’ projected areas were largest in the mist treatment with water and
no-water plants having similar areas. In contrast, the common D. caespitosa and D. p.
pulverulenta tended to have larger projected areas when watered (for D. lanceolata, mist
and water projected areas were similar) and the common species had the smallest
projected areas when not watered. This difference in effect of the water treatments on the
species was significant (P < 0.001, F = 13.474, df 16, 712).
A two-way ANOVA was done to test for effects of treatment and species on plant
size. The treatment × species interaction was significant (P < 0.001). The analysis was
further broken down by doing separate ANOVAs for each species comparing the effect
of treatments in pairwise comparisons (mist – water; water – no water; mist – no water).
For D. p. pulverulenta all combinations of treatments were significantly different from
each other. For D. verityi the only treatments that were not significantly different from
each other were between water and no water. For D. caespitosa the only treatment
combination that was not significantly different was mist and no-water. For D. c.
marcescens and D. c. agourensis, only the mist and no-water treatments were
significantly different from each other. For D. a. parva the only significant differences
were for the mist and water treatments. Finally, for D. b. blochmaniae, D. c. ovatifolia,
and D. lanceolata none of the treatments were significantly different.
70
mist – water .065
water – no water .564
mist – no water .346
14
sqrt projected surface area
.001
.428
.028
.348
.478
.035
<.001
.700
<.001
.080
.745
.012
<.001
<.001
<.001
.706
.429
.104
.001
<.001
.084
no water
mist
12
a
.171
.098
.001
water
10
8
6
4
df MS
Treatmt 2 77.561
Species 8 524.139
T*S
16 22.649***
Error 712 1.681
2
0
bloc marc parv ovat veri agou
n = 87
84
90
84
75
90
PULV LANC CAES
78
87
87
Figure E-2. Plant size affected by treatment and species. Projected surface areas of Dudleya plants sown
from wild collected seeds grown from summer 2006 to spring 2008 in three different watering treatments:
no-water plants received only natural precipitation, mist plants received misting during the four warmest
hours of the day in addition to natural precipitation, water plants were watered weekly. Data are from April
2007 and were square root transformed. Tukey probabilities are shown above. Inset: two-way ANOVA
(***P < 0.001).
All of the species showed a decline in yield values for the no-water group from weeks 2
to 6 (late August to late September: Figure E-3). Dudleya a. parva showed the greatest
decline (this is the time of year when leaves would not be present in wild populations of
this species). In the mist group only D. a. parva showed a lesser but similar decline in
yield readings, and D. verityi and D. p. pulverulenta showed a small decline from week 4
to 6. The water group yield readings showed no overall decline from weeks 2 to 6,
though, D. caespitosa and D. p. pulverulenta did show very slight decreases from week 2
to 4, but their yield readings increased from week 4 to 6. From weeks 10 to 12 (late
71
October to early November) all of the species and treatments except for the mist groups
of D. c. ovatifolia and D. lanceolata showed a decline in yield readings. All treatment
groups for all of the species showed a decrease in yield readings from weeks 14 to 16
(mid-November to early December) and in the mist group also from weeks 16 to 18
(early to mid-December). From weeks 22 to 30 (January through March) all of the
species in all of the groups showed a steep downward trend in yield values. Otherwise the
species responded differently to the different treatments and over the yield reading
period. The watering treatments affected the yield readings differently over time
(interaction P < 0.001, F = 24.295, df 26, 182). Yield readings differed over time (P <
0.001, F = 50.278, df 13, 91) and by treatment (P < 0.001, F = 76.163, df 2, 14). There
were no clear differences in the responses of the rare species compared to the common
species to any of the watering treatments.
In interpreting this experiment, it would be important to know whether misting
provided water to the plants’ roots or only cooled and humidified the air. A side
experiment was done to study this. Four-inch plastic pots were filled with the same
potting mixture the plants were potted in. They were weighed, placed in a drier at 100o F
for two days, and then weighed again. Eleven pots were placed randomly in the mist
group flats, and 11 in the no-water group flats. Pots were re-weighed in the evening 3, 8,
and 10 days later. The pots were then placed in the drier to dry for 4 days, were weighed,
and allowed to dry 3 more days when a final weight was taken. The weights of the soilfilled pots were normalized by dividing weights measured later by initial weights. t-tests
were used to determine if mist group soil was becoming wet by comparing the
72
Effective Quantum Yield
100
90
80
70
60
50
40
mist
water
A parv
no water
B veri
30
Effective Quantum Yield
100
90
80
70
60
50
40
C marc
D ovat
E agou
F LANC
G CAES
H PULV
30
Effective Quantum Yield
100
90
80
70
60
50
40
30
Effective Quantum Yield
100
90
80
70
60
50
40
S
A
O
N
D
J
F M
S
A
O
N
D
J
F M
30
0
2
4
6
8 10 12 14 16 18 20 22 26 30
week of measurement
73
0
2
4
6
8 10 12 14 16 18 20 22 26 30
week of measurement
Figure E-3. Effective quantum yield readings over time by species in three watering treatments. Siblings of
each species were randomly placed in three different watering treatments. Mist plants received misting
during the warmest four hours of the day and natural precipitation. Water plants received water weekly.
No-water plants received only natural precipitation. Effective quantum yield readings were taken after
plants had been placed in a greenhouse for at least 2 ½ hours. Most or all of the readings for each treatment
were taken on the same day with different treatments being measured on subsequent days over a period of
two to three days. Readings were taken from August 2006 to March 2007. Each reading consisted of six
measurements on different parts of the rosette. The graphs show the second highest reading averaged for
each species and the week readings were taken.
74
proportional pot weights between the mist and no-water group (Figure E-4). There were
no significant differences in the proportional weights of pots in the two water treatments,
although inexplicably the misting treatment did seem to be more variable than the nowater treatment.
0.998
misted
not watered
mass / starting mass
0.996
0.994
0.992
0.99
0.988
0.986
am
pm
pm
pm
pm
day 1 day 1 day 3 day 8 day 10
dried
Figure E-4. Proportions of soil filled pot weights placed in the mist and no-water treatment bays. Pots (n =
11 for each treatment) were filled with soil, placed in a drier to dry, weighed, and then placed randomly in
flats in the treatment areas. Weights were recorded in the morning and evening of day 1, the evenings of
day 3, 8, and 10, and after the pots were placed in a drier and had completely dried. Proportions were
calculated by dividing the weights over time by the starting weights. Standard error bars are shown.
75
Appendix F: Differences between confusable taxa
Table 1 in the thesis describes some characteristics that differentiate the species.
Petal color is often helpful for species identification. Colors range from white to shades
of yellow to red, some with distinguishing stripes of a color different from the
background color or glaucous keels. Other distinguishing features are the time of year
when leaves are present, the number of rosettes, and formation of protective coatings on
the leaves (Nakai 1987, Nakai 1983, Moran 1951, pers. obs.). Dudleya b. blochmaniae
has the habit of dying back during the summer to underground corms, and thereby
belongs to the subgenus Hasseanthus, whereas the other eight species belong to the
subgenus Dudleya. Among those eight, the most obvious distinction is between D. p.
pulverulenta, with its large body size and chalky covering, versus the other seven.
Among those seven, there are two cases where each species’ distinctiveness has been
questioned.
(1) Dudleya c. agourensis has been variously considered to be the same as D. c.
ovatifolia (Uhl and Moran 1953), a form of D. c. ovatifolia (Nakai 1983), or a subspecies
(Nakai 1987). Dudleya c. ovatifolia as narrowly defined is distinguished from D. c.
agourensis by its leaf undersides being maroon in color, having ovate to elliptic shaped
leaves, an unbranched caudex, petal apices that spread 90o or more, and slightly longer
pedicels (Nakai 1987).
(2) Dudleya lanceolata and D. caespitosa appear very similar and belong to a
polyploidy complex that might intergrade. Dudleya lanceolata is distinguished from D.
caespitosa by having a simple or little-branched caudex rather than a branching one that
can form over 100 rosettes, a different leaf shape, having a gently curved rather than an
76
obpyramidal shaped inflorescences (Moran 1951), and 34 chromosomes rather than 51
(Uhl and Moran 1953).
In the course of doing the thesis, data were gathered for many characters that
might differ between these confusable species. For continuous characters, like various
aspects of size, two-sample tests were done in the spirit of planned comparisons using
only the data on D. c. ovatifolia versus D. c. agourensis, and then only the data on D.
lanceolata versus D. caespitosa. This was done for the many variables for which larger
analyses mentioned in the thesis had been performed, e.g., nested ANOVAs. Replicated
G2 tests-of-independence were done to compare species for % reproductive. Analyses
that involved interactions such as the coastal versus inland analyses, were re-run with
only two species, and the species × site interaction or the species × site × date interaction
are reported. The root cross-sectional area of D. caespitosa #25 in the coastal garden was
winsorized. Table F-1 reports on the two “planned” comparisons.
As regards the habitat differences between D. c. ovatifolia and D. c. agourensis,
there were no significant differences in slope or in nearest neighbor distance but there
was in aspect. The life-history traits longest leaf length, leaf number, inflorescence
height, fruit number, seed projected area, and percent seedling survival were significantly
different but seeds per fruit, and percent seed germination were not. Dudleya c. ovatifolia
had smaller and fewer leaves, shorter inflorescences, fewer fruits, smaller seed projected
area, and lower percent seedling survival than D. c. agourensis. Leaf size of plants grown
in the coastal and inland gardens differed significantly between gardens and over time,
but rosette weights and root-crown cross-sectional areas of plants grown in the
77
Table F-1. Planned comparisons of species sometimes considered indistinct. For interactions, numbers
reported are differences between means, coastal - inland; for example, this entry represents Y’ of coastal D.
c. ovatifolia – Y’ of inland D. c. ovatifolia versus Y’ of coastal D. c. agourensis – Y’ of inland D. c.
agourensis.
D. c. ovatifolia vs.
D. c. agourensis
Habitat variables
Slope, degrees
Nearest same species
neighbor distance, cm
Aspect
Life-history variables
Longest leaf length (log)
Leaf number (sq rt)
Inflorescence height
(log)
Fruit number (cube rt)
Seeds per fruit (-1/6)
Seed cross-sectional
surface area, mm
% germination (arcsine)
% seedling survival
root:shoot (log)
10-90 vs. 25-90
25.8 vs. 68.3
0-180o vs. 90-0340o
1.8 vs. 2.6
5 vs. 10
11 vs. 26 cm
19 vs. 74
52 vs. 62
0.254 vs. 0.288
59 vs. 64
81 vs. 92
-0.597 vs. -0.409
Coast/inland interactions with species
Rosette weight g,
0.2844 vs 0.3288
sqrt(Y+.5)
Root crown x-sectional
0.0252 vs. 0.0167
area cm2, log (Y+1)
% Reproductive
4.8 vs 0.1
P
F (df)
P = 0.148
2.154 (1, 58)
P = 0.436
0.617 (1, 58)
P < 0.001
113.506 (1, 58)
P = 0.001
11.323 (1, 58)
P < 0.001
76.418 (1, 58)
P < 0.001
92.161 (1,58)
P < 0.001
65.415 (1,58)
P = 0.966
0.002 (1,57)
P = 0.012
7.619 (1,20)
P = 0.137
2.242 (1, 115)
P < 0.001
17.579 (1,115)
P = 0.004
8.867 (1,51)
P = 0.580
0.309 (1,101)
P = 0.505
0.448 (1,100)
Test not reliable
Leaf size log(Y+1)
see Figure 6 P < 0.001
Spp x garden x date
8.427 (7, 749)
Watering treatment interactions with species
Projected SA, sqrt cm2
0.330 vs 0.249 P = 0.859
Water – no_water
0.032 (1, 109)
Projected SA, sqrt cm2
0.719 vs 0.990 P = 0.525
Mist – no_water
0.406 (1,110)
Photosynthetic activity
see Figure E-3 P = 0.042
Spp x treatment x date
1.529 (26, 2145)
78
D. lanceolata vs.
D. caespitosa
0-90 vs. 0-90
168 vs. 50.8
50-0-140o vs. 230-0320o
3.8 vs. 6.4
7 vs. 16
69 vs. 49
83 vs. 88
123 vs. 58
0.369 vs. 0.427
80 vs. 73
96 vs. 94
-0.287 vs. -0.415
0.2297 vs 0.5059
-0.0188 vs. -0.009
-7 vs -10
see Figure 6
0.533 vs 2.628
0.874 vs 0.965
see Figure E-3
P
F (df)
P < 0.001
27.996 (1, 58)
P = 0.028
5.103 (1, 58)
P = 0.089
2.994 (1, 58)
P < 0.001
56.203 (1, 58)
P < 0.001
92.982 (1, 58)
P < 0.001
14.540 (1,58)
P = 0.820
0.052 (1, 58)
P < 0.001
24.515 (1,57)
P = 0.002
12.841 (1, 20)
P = 0.035
4.550 (1, 113)
P = 0.033
4.642 (1, 113)
P = 0.005
8.362 (1, 55)
P = 0.186
1.769 (1,114)
P = 0.843
0.039 (1,114)
P = 0.769
G2hetero=0.086 (1)
P = 0.002
3.210 (7,798)
P = 0.002
10.489 (1,108)
P = 0.872
0.026 (1,112)
P = 0.233
1.190 (26, 2184)
gardens were similar. Differences between percentages of individuals reproductive in
each of the gardens were not tested because the percentages were near 100%. The size of
plants grown in the different watering treatments, as measured by projected surface areas,
did not differ between the water and no-water treatments nor between the mist and nowater treatments. In terms of reproduction in the watering treatment, there was no
significant difference in the first spring. The second and third springs were not tested
because the test is not reliable for percentages near 100%.
Comparing D. lanceolata versus D. caespitosa, substrate slope and nearest
neighbor distance were significantly different, but aspect was not. Dudleya lanceolata
and D. caespitosa showed significant differences in longest leaf length, leaf number,
inflorescence height, seeds per fruit, seed projected area, percent seed germination, and
percent seedling survival but not number of fruits. Dudleya lanceolata had smaller and
fewer leaves, longer inflorescences, more seeds per fruit, smaller seed projected areas,
and greater percent seed germination and percent seedling survival than D. caespitosa.
Plants grown in the coastal and inland gardens showed significant differences in linear
leaf lengths between gardens over time, but there were not differences between rosette
weights, root-crown cross-sectional areas, or percent of individuals reproductive.
Projected areas of plants grown in the different watering treatments differed between the
water and no-water groups. Dudleya caespitosa, which was not prone to flowering,
responded to water much more strongly in terms of projected area than D. lanceolata,
which were more likely to flower. There was no significant difference between the mist
and no-water groups. Differences between D. lanceolata and D. caespitosa were
heterogeneous in bolting behavior between the watering treatments in the third spring,
79
with D. lanceolata being more likely to bolt (Figure F-1). Differences in bolting behavior
in the first and second springs were not tested because percentages were close to 0 or
100%.
1
mist
0.9
water
0.8
nowater
% Reproductive
0.7
0.6
G2
df
P
mist
25.22
1
<0.001
water
10.37
1
0.001
0.3
no water
52.14
1
<0.001
0.2
total
87.72
3
<0.001
0.1
pooled
75.13
1
<0.001
heterogeneity
12.60
2
0.002
0.5
0.4
0
LANC
CAES
Figure F-1. Bolting in the third spring for D. lanceolata and D. caespitosa in the three watering treatments.
Sibling plants were randomly placed in three different watering treatments: water, mist, and no-water.
Water treatment plants received natural precipitation or water weekly. Mist group plants received misting
the four warmest hours of the day and natural precipitation. No-water plants received only natural
precipitation. Presence of inflorescences was recorded each of three springs. Percent of reproductive
individuals was calculated by dividing the number of individuals per species in each watering treatment
with inflorescences by the total number of individuals in each species in each watering group. All n = 29
plants per species per treatment.
Considering all of the habitat and life-history characters measured, each species
was distinct from every other species in multiple traits. The comparisons between D. c.
ovatifolia versus D. c. agourensis and D. lanceolata versus D. caespitosa support the
view that each species is unique. In contrasting D. c. ovatifolia and D. c. agourensis,
there were significant differences in one of the three habitat characteristics and six of the
eight life-history characteristics measured. In contrasting D. lanceolata and D.
caespitosa, two of the three habitat characteristics and six out of eight life-history
80
characteristics were significantly different between the species. True, statistical
significance is not the same as 100% discriminate distinctiveness, but the species can be
identified based on single characters (such as color and amount of branching), and the
large number of other characters that tend to differ confirm that these key characters are
indicative of differentiation between lineages.
81
Appendix G: Management implications and recommendations
This thesis is an important step in learning about the life-histories and other
factors that affect the prevalence and persistence of rare Dudleya species in the Santa
Monica Mountains region. However, more needs to be known in order to improve plans
for their conservation. Factors that have been found to influence the prevalence of the
rare species are that they produce fewer fruits, fewer seeds per fruit, smaller seeds, are
smaller in size, have shorter inflorescences, require co-occurring vegetation to be of a
lower stature, milder microclimates, and aspects facing closer to north than the common
species. The rare species also seem to depend on the presence of mosses, lichens, and/or
Selaginella.
The life-history traits of the rare species affect their ability to increase population
size and disperse into other habitats. Therefore, a recommended follow-up to this study
should be the establishment of a long-term demographic monitoring program. Monitoring
is necessary in order to ascertain if the rare species’ populations are increasing, stable, or
in decline. Monitoring would also allow for the determination of which life stages are
most critical so that conservation efforts could be concentrated on those stages (Elzinga
et al. 1998). Specifically, it would be useful to know if mortality is mainly in the first few
months after germination, during the remaining time period until first-reproduction, or
between subsequent reproductive bouts. It would also be desirable to determine whether
factors associated with mortality differ among the various rare and common Dudleya
species. In conjunction with the monitoring, a seed longevity study should be conducted
in order to determine if these species have a seed bank and the number of years the seeds
are viable (Elzinga et al. 1998). This information will make it possible to perform
82
population projections alerting mangers of potential declines before they occur (Elzinga
et al. 1998). Once there is better understanding of the rare species’ demographics,
supplemental research projects could be done. If populations are in decline, it would be
important to know if, in a metapopulation sense, some were sources and others sinks. It
would be a good idea to look at the genetic make-up of each grouping of species to
determine population and possibly meta-population structure. If number of viable seeds
being produced or seedling survival were critical for population stabilization then a study
of pollination services could determine the need for supplemental manual pollination
(Levin and Mulroy 1985). If it were determined that seedling establishment is a critical
stage for population persistence, then seeds from declining populations could be collected
and sown in captivity. The resultant plants could be cross pollinated with each other
(derived from the same population) and those seeds could be put back into the natural
population to augment seed production and improve seedling establishment (Pavlik
1997).
A better understanding of the rare species’ habitat requirements could also be
used to identify suitable habitats for the establishment of new populations. This study and
personal observations indicate that population size is dependent on the availability of
places for seedling establishment and probability of recruitment. Understanding the
importance of bryophytes, lichens, and/or Selaginella for seedling establishment is
critical. Observations could be made to verify this dependence. Furthermore, the rare
species’ populations are denser than those of the common species in part because of the
increase in suitable habitat where mosses, lichens, and/or Selaginella are present. It
would be important to know if there were a tradeoff between density and interspecific
83
competition. If density is found to have a significant effect, determination of density
thresholds for each species would be valuable. In this way population sizes could be
maximized if seed augmentation or introduction projects were undertaken.
Habitat protection efforts should also be enacted. Species that are locally abundant and
adapted to specialized habitats may be able to persist as long as those habitats exist
(Levin 2000). It will be important, then, to monitor usage of the habitats where these
populations occur in order to prevent destruction (Lavergne et al. 2004, Lloyd et al. 2003)
that could negatively impact the rare Dudleya species growing there.
84