Table Of ContentMadrono, Vol. 52, No. 1, pp. 46-52, 2005
HERBIVORY AND THE ENDANGERED ROBUST SPINEFLOWER
(CHORIZANTHE ROBUSTA VAR. ROBUSTA)
Sandra Baron and Shannon M. Bros
•
Department of Biology, San Jose State University, San Jose, CA 95192-0025
Abstract
Insect herbivory has been shown to have substantial impacts on plantgrowth andreproductioninmany
systems. However, the effect of insect herbivores on rare and endangered plants has not been widely
studied, even though natural limitations on growth and reproduction, in combination with anthropogenic
changes in habitat quality and quantity, likely contribute to population decline. In the current study, an
insect exclusion experiment was used to assess the effects of insect herbivory on a federally listed
endangered annual plant: Chorizanthe robusta van robusta (Polygonaceae). The primary insect herbivore
was a microlepidopteran larva, an undescribed species ofAroga (Gelechiidae). Excluding Aroga larvae
led to a 30% increase in seed output compared to watercontrol. No change in plant survivorshiporseed/
flower ratios was found with insect exclusion. Control plants given supplemental water had increased
seed production, but only in the absence ofAroga infestation, an indication that infested plants could not
fully exploit additional resources. These results show that rare annuals are potential host plants forinsect
herbivores, and herbivory is an important factor to consider when evaluating endangered plant popula-
tions.
Key Words: insect exclusion, rare plants, sand dunes, Aroga, Gelechiidae.
Endangered plants characteristically have popu- this effect (Crawley and Gillman 1989; Maron and
lations that are limited in size and extent, often due Gardner 2000). However, research has shown that
to habitat loss caused by human activities. In coast- small populations of endangered plants can be re-
al areas of California, urban development and ag- stricted by low seed production (Pavlik et al. 1993;
riculture have reduced natural areas considerably. Bevill et al. 1999) so we can not discountherbivory
Under these conditions, any additional factor that when evaluating rare plants. Plants can be rare for
reduces survivorship or reproduction of a rare spe- a variety ofreasons (see Rabinowitz 1981), but the
cies can contribute to the possibility of extinction. end result is often small population size. Projec-
Numerous studies have shown that insect herbi- tions of population growth or decline are impossi-
vores reduce survivorship, growth, and reproduc- ble to make without first identifying the factors
tive output of plants (Rausher and Feeny 1980; which reduce plant survivorship and reproduction,
Louda 1982, 1984; Crawley 1983, 1989). In many and discerning the vulnerable life stages (Pavlik et
cases plant fecundity is more dramatically limited al. 1993; Schemske et al. 1994).
by herbivory than is survivorship, and an increase Excluding herbivores from a subset ofplants and
in seed number is often found when herbivores are comparing plant performance is the best way to as-
excluded, even when herbivory is at very low lev- sess the effects of herbivory in wild plant popula-
els (Crawley 1983; Kinsman and Piatt 1984; Brown tions (Crawley 1989), and this was the method used
et al. 1987; Root 1996; Wise and Sacchi 1996; for this study. Plant competition and availability of
Mauricio 1998; Parmesan 2000; Maron 2001). Leaf resources must also be considered, as these factors
and flower damage from herbivory can also indi- can work in concert with herbivory to affect plant
rectly affect seed production by decreasing polli- growth and reproduction. For example, limited re-
nation rates (Mothershead and Marquis 2000). Al- sources can increase the effect of herbivory on in-
though these effects of herbivory on plant perfor- dividual plants by restricting growth (Louda 1984;
mance are well documented, the question of how Louda et al. 1990), but some studies have shown
herbivores affect plant populations is still widely that even when resources are plentiful, plants can-
debated (Crawley 1983, 1989; Carson and Root
not overcome the effects of herbivory, especially
2000). Some studies have shown that a reduction annual plants (Pavlik et al. 1993; Wise and Sacchi
in seed by herbivores is likely to lead to a reduction
1996).
in plant abundance (Louda 1982; Louda and Potvin
1995; Wise and Sacchi 1996; Fagan and Bishop The current study seeks to determine if insect
herbivory reduces survivorship, growth, and seed
2000; Maron 2001), but density-dependent mortal-
output ofChorizanthe robusta var. robusta C. Parry
ity or a shortage of germination sites can negate
(Polygonaceae), a federally listed endangered plant.
Mammal herbivores are often important in sand
' Current address: 119 Rancho Road, Watsonville, CA dune habitats (Palmisano and Fox 1997); however,
95076-9608. e-mail: [email protected] no mammal herbivory was seen in preliminary
2005] BARON AND BROS: HERBIVORY AND AN ENDANGERED SPINEFLOWER 47
studies on C. robusta at two sites over two years Study Site
(personal observation), and Swank and Oechel
(1991) noted that rabbits rarely grazed Chohzanthe Sunset State Beach was selected as the location
for this study because the largest known population
fimbriata and C. polygonides in their study in chap-
of C. robusta (many thousands of plants) occurs
arral. Consequently, only insects were excluded in
over a wide area on the rear dunes. Sunset State
this study.
Herbivore density can vary between small and Beach is located in central California just west of
the town ofWatsonville (36°52.89'N, 121°49.69'W).
large patches of host plants (Bach 1988). Because
The study site was within a 300 square meter area
herbivore density patterns are an important factor
on the top ofareardune. These reardunes are stable
in predictive models, the relationship between
and dominated by coastal scrub species such as Er-
clearing size and herbivory was also investigated.
icameria ericoides (Less.) Jepson (Asteraceae). The
habitat is a mosaic of various sized openings be-
Methods
tween shrubs with sand, moss, grasses, bracken fern,
and forbs. Chorizanthe robusta grows in dense
Plant Species
patches in these openings. Much of the study site is
Chohzanthe robusta var. robusta is an annual colonized by Syntrichia princeps (De Not.) Mitt
spineflower that inhabits sandy soil sites in Santa [Tortula princeps], a low growing moss that forms
Cruz County, CA. Plants are low-growing and ex- mats in which C. robusta and other forbs grow.
tremely variable in size, forming a single upright The central coast of California has a moderate
stem or having multiple branches. Chorizanthe ro- mediterranean climate. During the study period
busta germinates in the winter and flowers from (October 2000-April 2001), the average monthly
April through June or July. Each plant produces temperature of 12°C was normal for this period. An
multiple small flowers and each flower can pro- average monthly rainfall of 2.4 inches was 79% of
duce one seed. Seeds are dispersed in involucres normal for this period. The last measurable rainfall
with hooked awns that can attach to passing ani- for the season was on or about April 18, 2001 (U.S.
mals. Chorizanthe colonizes along trails and in Dept. of Commerce 2002).
clearings over the landscape. At the study site,
some of these clearings are very large with thou- Experimental Design
sands of plants and others are small with only a An insect exclusion experiment with three treat-
few individuals encircled by shrubs. This plant is ments was performed to assess the effects of her-
federally listed as endangered and is known from bivory on plant survivorship, plant size, and seed
seven populations, some less than 100 plants output. In one set of plants insects were excluded
(USFWS 2000). The genus Chorizanthe is taxo- by using an insecticide spray, Carbaryl (1-naphthol
nomically challenging, with many closely related A^-methylcarbamate), a ready-mixed aqueous solu-
species, subspecies, and varieties in California tion of a wide-spectrum carbamate insecticide,
(Ertter 1996). There are taxonomic uncertainties brand name Sevin (Rhone-Poulenc). Carbaryl kills
about C. robusta at the study site due to the prox- chewing insects for three to ten days, and has a half
imity ofa closely related species Chorizanthepun- life of seven days in aerobic soil (PMEP 1993).
gens (Benth). Chorizanthe pungens is thought to Prior studies on this insecticide indicate that its ef-
grow primarily on the fore dunes and Chorizanthe fects on plant growth are minimal (Jones et al.
robusta primarily on the rear dunes; however, no 1986; Gibson et al. 1990). Because spraying ofwa-
published studies have quantified the genetic ter may influence growth and seed production, two
structure of the species complex. The plants cho- controls were included to assess the effect ofinsect
sen for this study were on the rear dunes and mor- exclusion with an insecticide independent of spray-
phologically similar to Chorizanthe robusta var. ing. The first control included plants that were
robusta at other sites. sprayed in the same manner as the insecticide but
with water only. For the second control, the plants
Insect Herbivore were not sprayed. Every seven to ten days from
March 17 to May 14, 2001, until plants were in
Although this study examined the effect of ex- flower, insecticide and water spray treatments were
cluding all chewing insects, the primary insect her- applied in the morning when winds were calm and
bivore on C. robusta were larvae ofan undescribed temperatures low.
moth species in the genus Aroga (Gelechiidae) (J. A randomized block design was used to mini-
Powell personal communication). These larvae cre- mize effects from microhabitat variation. Fifty
ate silken shelters covered with sand and litter, at- blocks, each with three plants of similar size grow-
tached to the base of C. robusta plants. They feed ing near each other, were randomly selected. Each
on leaves and are active from March through June. plant in the block was assigned a different treat-
Pupation occurs in shelters on or near the soil sur- ment, and the order ofassignment was randomized.
face. Adult specimens were collected in the field in Four types of measurements were made. Plants
early August. were inspected weekly for the duration ofthe study
MADRONO
48 [Vol. 52
Table 1. Randomized Complete Block ANCOVA for Testing the Effect of Excluding Insect Herbivores on
Number of Seeds per Plant. Independent variable was Treatment with three levels. Insect exclusion (IE), Waterspray
control (W), and Non-spray control (N). Dependent variable was number of seeds per plant (In transformed). Blocks
were randomly selected groups ofthree plants. Covariate was final plant density.
Source SS df MS F P
Treatment 9.401 2 4.700 3.657 0.038
W
WIE vs. 7.305 1 7.305 5.683 0.023
vs. N 0.004 1 0.004 0.003 0.956
Block 31.478 16 1.967 1.530 0.151
Final Plant Density 8.983 1 8.983 6.989 0.013
Error 39.848 31 1.285
to monitor survivorship and determine whether variables. Final plant density was included as a
they had been infested withAroga. Local plantden- covariate.
sity was measured at the beginning and end of the To evaluate the effect of plant patch size on
experiment by positioning each study plant in the sources ofherbivory, 145 plants in patches ofvary-
center of a 10-cm square, and counting all plants ing sizes were examined throughout the study pe-
within the square. In addition, the size of each riod. Patches were identified as groups of plants
clearing (with study plants) was measured. After surrounded by shrubs. The area of each patch was
seed set, plants were collected to measure plant measured in square meters (length X width). Patch-
size, number of seeds, and number of flowers. Be- es were classified by area into three groups: Small:
cause Chorizanthe robiista has small sparsely dis- 0-3.00 m^. Medium: 3.01-7.00 m% and Large:
tributed leaves along with highly variable stems and 7.01-10.00 m^. Evidence of rabbit grazing and in-
branches, the sum ofthe length ofall branches plus festation by Aroga was recorded for each patch. A
the length of the stem was used as a measure of 2X2 Test of Independence (Zar 1996) was used to
plant size. For each plant, seed/flower ratios were determine if there was a relationship between the
also computed. presence or absence of rabbit grazing and patch
Randomized Complete Block Analysis of Co- size. The same type of test was used to determine
variance (Zar 1996) was used to assess the effect if the presence or absence ofAroga larvae was in-
of excluding insect herbivores on plant size (total dependent of patch size.
length ofbranches plus stem), numberofseeds, and
seed/flower ratios. For all analyses, the independent Results
variable was Treatment with three levels, insect ex-
clusion by application of insecticide, water spray Plant mortality was extremely low during this
control, and the non-spray control. Plant size and study. Only two (out of 150) study plants died and
number of seeds were transformed for analysis as both were due to gopher activity. However, rabbits
ln(x) because variances of the untransformed vari- (Sylvilagits bachmani Grinnell and Storer) removed
ables were not homogeneous among treatments. mature seed heads late in the season from 11% of
Blocks in the analyses were the randomly selected study plants, effectively eliminating their reproduc-
groups ofplants. To insure that the treatments with- tive potential.
in a block really represented cases where herbi- The RCB ANCOVA showed that seed number
vores were excluded or not, only those blocks in increased when insects were excluded (Table 1).
which Aroga occurred were considered for analy- The first a priori comparison showed that mean
ses. Blocks in which one or more plants died or in number of seeds per plant (In transformed) was
which grazing by rabbits occurred during the ex- greater (P < 0.023) in the insect exclusion treat-
periment were also excluded from analyses. For ment as compared to the water spray control (Fig.
each dependent variable, two a priori comparisons 1). The second a priori comparison showed that
were performed to compare treatments. To assess mean number of seeds per plant did not differ (P
whether the application ofinsecticide affected plant = 0.956) between the water spray control and the
size or number of seeds, the insect exclusion treat- non-spray control (Fig. 1). The block effect was not
ment was compared to the water spray control. Be- significant (P = 0.151) indicating that a block de-
cause final plant density was correlated with plant sign was not necessary. However, final plant den-
size (r = -0.493) and number ofseeds (r = 0.484), sity was a significant covariate (P = 0.013). AN-
final plant density was included in the analyses as COVA for seed/flower ratios showed no significant
a covariate. To determine if there was a difference difference among treatments (P = 0.211).
in the effect of watering between infested and non- The results for plant size were similar to the re-
infested plants, all watered plants were analyzed us- sults for number of seeds (Table 2). The RCB AN-
ing ANCOVA with Infested as the independent var- COVA showed that plant size increased when in-
iable, and seed number and plant size as dependent sects were excluded. The first a priori comparison
1
2005] BARON AND BROS: HERBIVORY AND AN ENDANGERED SPTNEFLOWER 49
6
Insect Water spray Non-spray
Insect Water spray Non-spray
exclusion control control
exclusion control control
Fig. 2. Mean plant size per plant (cm) (In transformed)
Fig. 1. Mean numberofseeds perplant (In transformed) for the three treatments. Insect exclusion. Water spray
for the three treatments. Insect exclusion. Water spray control, and Non-spray control, adjusted for final plant
control, and Non-spray control, adjusted for final plant density. Error bars are 95% confidence limits.
density. Error bars are 95% confidence limits.
sprayed with insecticide had signs of Aroga infes-
pslhaonwte(dInthtartamnsefaonrmleedn)gtwhaosfgbrreaantcehres(Ppl<us0s.t0e2m6)peirn tation and Aroga larvae tended to appear in larger
the insect exclusion treatment as compared to the patches of plants (Fig. 5).
water spray control (Fig. 2). The second a priori Discussion
comparison showed that mean length of branches
plus stem per plant did not differ (P = 0.273) be- The results of this study indicate that insect her-
tween the water spray control and the non-spray bivores significantly reduced both size and lifetime
control. The block effect was barely significant (P seed production of these annual plants, factors that
= 0.050) indicating that a block design was desir- could have far reaching effects on a small popula-
able for experiments in which plant size was the tion (Table 1). Since seed/flower ratios did not dif-
measured variable. As with the analysis for number fer for insecticide treated plants, insects reduced
of seeds, final plant density was a significant cov- seed production by reducing plant size (or resource
ariate (P = 0.040). allocation) rather than pollination rates. Plant size
The effect of watering differed for infested vs. has often been found to be correlated with seed
non-infested plants. Average seed number was sig- output (Rausher and Feeny 1980; Wolfe 1983;
nificantly higher for non-infested plants (P < 0.02) Brown et al. 1987; Stocklin and Favre 1994). Po-
and final density was an important covariate (Table tential growth effects from insecticide use mustalso
3, Fig. 3). be considered. In the absence of herbivory, insec-
Both rabbit grazing and presence ofAroga larvae ticide treated plants were no largeron average (16.8
appeared to be related to plant patch size. The re- cm) than plants sprayed with only water (17.2 cm).
sults of the 2X2 Test of Independence showed that Because other studies have shown that Carbaryl has
plant patch size was related to the presence or ab- a negative or minimal effect on plant growth (Jones
sence of rabbits (Log-likelihood ratio = 23.508, df et al. 1986; Gibson et al. 1990) it is unlikely that
= 2, P < 0.001); rabbit grazing tended to occur Carbaryl induced plant growth in this study.
more often in the smallest plots (Fig. 4). Patch size Additional water increased seed output, but only
was also related to the presence or absence of Ar- in plants without Aroga infestation (Fig. 3). Other
oga larvae (Log-likelihood ratio = 9.415, df = 2, studies have also found that abundant or supple-
P < 0.010). During this study, 34% of plants not mental water did not produce an increase in seed
Table 2. Randomized Complete Block ANCOVA for Testing the Effect of Excluding Insect Herbivores on
Plant Size. Independent variable was Treatment with three levels. Insect exclusion (IE), Water spray control (W) and
Non-spray control (N). Dependent variable was total branch length plus stem per plant (In transformed). Blocks were
randomly selected groups of three plants. Covariate was final plant density.
Source SS df MS F P
Treatment 2.237 2 1.619 6.09 0.006
W
WIE vs. 1.449 1 1.449 5.454 0.026
vs. N 0.331 1 0.331 1.245 0.273
Block 8.424 16 0.527 1.981 0.050
Final Plant Density 1.223 1 1.223 4.602 0.040
Error 8.239 31 0.266
MADRONO
50 [Vol. 52
_
6 Rabbit grazed
Yes
UNO
Q) 3
Small Medium Large
Infested Non-infested Patch size
Fig. 3. Mean numberofseeds perplant (In transformed) Fig. 4. Plant patch size (small = 0-3.00 m^, medium =
ffoorrifinnfaelstpeldanvts.dennosni-tiyn.feEsrtreodrwbaatresrarsepr9a5ye%dcpolannftisd,eandcjeusltiem-d 3se.n0c1e-7o.f00ramb-b,itlagrrgaezi=ng.7.01-10.00 m^) vs. presence orab-
its.
output in plants subject to herbivory (Swank and
Oechel 1991; Pavlik et al. 1993; Wise and Sacchi cause proportionally greater threats to rare and en-
1996). Because Aroga larvae remove leaves, they dangered plant populations.
compromise the plant's ability to garner resources There was some evidence that herbivores were
(Louda 1984; Louda et al. 1990). This potential in- selecting plants based on an environmental condi-
teraction between herbivory and resource uptake tion: clearing size. Larvae were more often found
and allocation is an important factor to consider in in the largest clearings, and rabbit grazing was
rare plant management. If models are used to pre- more prevalent in small clearings and at the edges
dict plant population growth, it may be necessary where shrubs were dense (Figs. 4 and 5). Herbivore
to include potential differences in resource utiliza- density patterns will be important to include in pre-
tion by the proportion of the population subject to dictive models, but they may also have evolution-
insect herbivory. ary consequences. According to John Thompson
Decreased seed production is a potential threat (personal communication), selection based on an
to the long term viability of this plant population environmental variable can increase the potential
only if it is seed limited (Louda 1982; Crawley for genetic polymorphisms. In addition, the discov-
1983, 1989). A reduced seed supply may not affect ery of a possibly specialist herbivore presents fu-
a population with a shortage of "safe sites" for ture research opportunities that may help shed light
germination (Crawley and Gillman 1989). Howev- on Chorizanthe taxonomy. Evolutionary relation-
er, "safe site" availability can be difficult to deter- ships between species can evolve over small time
mine because it can vary over years and over the scales, even decades, and changes in the distribu-
landscape (Maron and Gardner 2000). In sand dune tion ofmetapopulations are one ofthe "normalpro-
habitats it is likely that the availability of germi- cesses of evolution" (Thompson 1998). More re-
nation sites fluctuate yearly due to shrub growth search is needed to determine if this moth species
and small scale disturbances. Research has shown is a specialist on Chorizanthe. Although it is un-
that annual plants in sand dune environments often usual for an annual plant to have a specialist her-
show evidence of seed limitation (Turnbull et al. bivore (Crawley 1983), most small moths are spe-
2000). Seed reduction can also have a greater im- cialists and they can survive in small habitat patch-
pact on a plant species, such as C. robusta, that has es (Powell 1999). In a study of the range size of
metapopulation dynamics (Bevill et al. 1999), de- host plants fora variety ofinsect herbivores inEng-
fined as sub-populations connected by dispersal land, Hopkins et al. (2002) found that a number of
(Eriksson 1996). Ecological factors such as these, "micro moths" were associated with rare plants.
combined with a loss of habitat due to human ac- Microlepidoptera such as these are not well studied
tivities, may intensify the effects of herbivory and and 50% to 90% of species with small adults col-
Table 3. ANCOVA for Testing the Effect of Water on Seed Number. Independent variable was Infestation with
two levels. Yes (Y) and No (N). Dependent variable was number of seeds per plant (In transformed). Covariate was
final plant density.
Source SS df MS F P
Y vs. N 8.857 1 8.857 6.094 0.020
Final Plant Density 29.770 29.770 20.483 0.000
1
Error 39.241 27 1.453
2005] BARON AND BROS: HERBIVORY AND AN ENDANGERED SPINEFLOWER 51
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