Host use and foraging in the parasitic plant Cuscuta subinclusa.
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Host use and foraging in the parasitic plant Cuscuta subinclusa
Kelly, Colleen Kay, Ph.D.
The Universi~y of Arizona, 1988
U·1rl-I 300 N. Zeeb Rd. Ann Arbor, MI 48106
HOST USE AND FORAGING IN THE PARASmC PLANT
CUSCUTA SUBINCLUSA
by
Colleen Kay Kelly
A Dissertation Submitted to the Faculty of the
DEPAR1MENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY
In Partial Fulfillment of the Requirements
For the Degree of
DOCTOR OF PHILOSOPHY
In the Graduate College
THE UNIVERSITY OF ARIZONA
1988 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Final Examination Committee, we certify that we have read the dissertation prepared by -"'Co:.:l=le:.;e"'nc.Ka=y-'K;:.:e:.:l"'ly'-______entitled Host use and foraging in the parasitic plant, Cuscuta subinclusa
(Convolvulaceae)
and recanrnend that it be accepted as fulfilling the dissertation requirement
Date Dr. mStrauss
Date S 3/ pg Date
Date
R n approval and acceptance of this dissertation is contingent upon the candidate's suJ::mission of the final copy of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and reconunend that it be accepted as fulfilling the dissertation reQUii;9LcQ
Dissertation Director Date 2
STATEMENT BY AUTHOR
TIlls dissertation has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.
Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. ACKNOWLEDGEMENTS
During the course of this work I received assistance from many people and organizations. Carol Augspurger advised me through my masters work and the initial, agonizing stages of Dodder Research; I'll never write a grant proposal without her looking over my shoulder, and I'll be the better for it. Pete Atsatt served as a de facto advisor in California, providing much invaluable input throughout. In the field, Charlotte Bontrager provided both quality and quantity time; the help of James Albert, Rick Hallowell, and Dan Gilmore shortened considerably the demographic work. Logistic support and camaraderie were generously supplied by Mary Jo Elpers, Charlotte and Dave Bontrager, Dana Echols, Pete Bloom, and Paul and Linnea Dayton. Paul Dayton also provided a desk at Scripps and a stimulating group of scientists with which to interact. I especially want to acknowledge Jeff and Martha Froke, and their generosity during my many months at Starr Ranch Audubon Sanctuary. Financial support was provided by NSF Doctoral Dissertation Improvement Grant BSR 84-01437, University of Illinois Biomedical Research Grant (with C. K. Augspurger), El Dorado Audubon Chapter, Association of Women in Science, Starr Ranch Audubon Sanctuary, University of Illinois Doctoral Dissertation Assistance, and several Sigma Xi Grants-in-Aid.
There was no deadwood on my dissertation committee and each member contnbuted significantly to my final product and to my growth as a scientist. My committee members were: James H. Brown, D. Lawrence Venable (co-dissertation advisors), Michael Rosenzweig, Richard Strauss, and Frank Telewski. I came to the University of Arizona to work with Jim Brown, and it's turned out to be one of the best professional decisions I've ever made. Although Astrid Kodric-Brown held no official position on my committee, my dissertation and my time at Arizona were significantly improved by her intellectual generosity and the pleasure of her friendship. Many thanks are due to Gordon Fox, Bob Holmes, and Wayne Spencer who read early drafts of everything and yet have remained cordial.
I'd like to note my appreciation for my mother, Betty J. Kelly, who performed exceedingly well the essential function of believing in me even when she had no idea what I was doing. And for my sister, Laurel, whom I wouldn't trade for any other. I should also mention here my brother David and his family, so they don't feel left out. Lastly, I am grateful to my oldest brother, Steven D. Kelly, from whom I received emotional and financial support throughout, and who usually managed to find time to listen to me when things got rough. He provided a safe place for me in this universe until his death from AIDS on 27 January 1987. TABLE OF CONTENTS
LIST OF ILUSTRATIONS ...... 7
LIST OF TABLES ...... 8
ABSTRACT...... 9
CHAPTER ONE
INDIVIDUAL RESPONSES TO RESOURCES: CUSCUTA SUBINCLUSA AS A FORAGER...... 11
Introduction ...... 11
Study site...... 13
Preuptake Response...... 14
Results ...... 17
Discussion ...... 18
Cost of Host Exploitation ...... 23
Results ...... 23
Discussion...... "...... 25
Host Value and Parasite Response...... 25
Immediate growth response ...... 28
Long-term growth response ...... 29
Parasite growth in nature ...... 32 Table of Contents (continued)
Results
Immediate growth response (10 day experiment) ...... 33
Long-term growth response (30 day experiment)...... ,...... 34
Parasite growth in nature ...... 41
Discussion
Host choice ...... 42
Coiling and uptake...... 45
Host quality and patch use ...... 45
Fitness ...... 48
Results ...... 49
Discussion ...... 50
Parasite Status and Coiling ...... 52
Results ...... 54
Discussion ...... 56
General Discussion ...... 58
Adaptation ...... 59
Variation in coiling response ...... 60
Conclusions ...... 61 Table of Contents (continued)
CHAPTER TWO
POPULATION LEVEL PATTERNS OF HOST USE BY CUSCUTA SUBINCLUSA: HOST ABUNDANCE AND SPATIAL ARRAY...... 64
Introduction ...... 64
Individual response ...... 65
Habitat trait5 ...... 66
Interaction ...... 67
Materials and Methods
Study site and study organism ...... 68
Host use...... 69
Parasite response to host species ...... 69
Host abundance ...... 70
Proximity to Malosma ...... 72
Results ...... 72
Discussion ...... 81
LITERATURE CITED ...... 88 LIST OF ILLUSTRATIONS
Figure 1: Transplant aparatus ...... 15
Figure 2: Time course for parasite coiling and formation of haustorial initials ...... 19
Figure 3: Parasite response to different host species ...... 21
Figure 4: Cost of coiling ...... 24
Figure 5: Marginal value of value theorem ...... 27
Figure 6: Number of haustoria as a function of length...... 35
Figure 7: Relationships between parasite response and potential reward derived from host ...... 37
Figure 8: Growth after 10 days ...... 39
Figure 9: Mean nitrogen content of hosts and parasite ...... 40
Figure 10: Relationship of mean size increase ...... 43
Figure 11: Parasite size and fitness ...... 51
Figure 12: Parasite stem width and nutritional status ...... 55
Figure 13: Parasite stem width and coiling response ...... 57
Figure 14: C. subinc/usa growth and phenology during a year ...... 71
Figure 15: Correlation between individual response ...... 73
Figure 16: Correlation of host abundance ...... 77
Figure 17: Correlation of average host use ...... 78
Figure 18: Correlation between species abundance ...... 79 LIST OF TABLES
Table 1: Summary of ANOVA, ANCOVA, and MANOVA results ...... 20
Table 2: Summary of correlation results ...... 36
Table 3: Categories of host cover index ...... 74
Table 4: Mean values of host use ...... 76 ABSTRACT
Foraging theory predicts active responses by organisms upon encounter with a resource, as opposed to the passive responses of differential survivorship and growth. Stems of the parasitic plant Cuscuta subinclusa (Convolvulaceae) discriminate among host species and invest in resource acquisition (coil) relative to hast quality in a way predicted by the marginal value theorem (MVT). The
MVT is used to describe patch tenure by foraging animals. C subinclusa can be said to forage in that: 1) stem coiling, the necessary antecedent and determinant
of resource uptake, precedes exploitation of host materials; and 2) mean coiling
on a host species is proportional to: a) mean growtb/haustorium (i.e. uptake
efficiency), b) mean biomass accumulation over the season, and c) mean parasite
growth/host individual. Parasite coiling js correlated with expected reward in
terms of growth/host individual for the 5 native host species examined, but not
when a non-native species is added to the model, which suggests coiling response
is a result of natural selection. Preliminary evidence indicates that coiling in C.
Sltbinciusa is induced by host bark chemicals. Resource-poor stems of C.
subinclusa are more likely to coil, and coil more, than resource-rich stems,
suggesting that nutritional state of the parasite as well as nutritional value of the
host affects foraging responses.
Although all stems coiled on host branches in the described transplant
experiments, evidence from other experiments suggests that the costs of growth,
or "searcb costs", may affect host acceptability. When water is readily available, 10 transplanted C. subinclusa stems are more likely to not coil in response to branches of Platanus racemosa. During the dry season, when cellular expansion is difficult, all P. racemosa branches were coiled upon. larger parasites are more likely to over-winter and set seed a second season than smaller, and parasites that start from over-wintered tissue are significantly larger at flowering than are those that have started from seed. Thus seed set is correlated with parasite size at the end of the season, linking the foraging response and fitness of the plant.
The descnoed individual level adaptation of C. subinclusa does not,
however, predict population level patterns of host use. Rather, the principal
determinant of host use by C. subinclusa is average proximity of a potential host
species to Malosma laurina (Anacardiaceae). Individuals of C. subinclusa infest
many host species over the course of the growing season, but at the study site,
initially establish, set the vast majority of seed, and over-winter only on M.
launna. Individual response of C. subinclusa contnbutes to the model of host use
only after the effect of proximity to M. laurina is accounted for, suggesting that
mechanisms that increase exploitation of a host take effect after contact between
host and parasite. Given that C. subinclusa operates at a scale similar to that of
many insect herbivores, the results suggest that juxtaposition of potential host
species may have a significant effect on diet in other non-monophagous,
herbivorous species. 11
CHAPTER ONE
Individual responses to resources: Cuscuta subinclusa as a forager
INTRODUCTION
Foraging theories are constructed to describe how animals search for, pursue, and capture prey. The goal of these theories has been to detennine how these behaviors are changed to respond to variation in characteristics of the prey
(Schoener 1971; Pyke et al 1977; Krebs et al. 1983; Pyke 1984; Stephans and
Krebs 1987). The thesis of this paper is that this set of theories which originated in the study of the behavioral and evolutionary ecology of animals (Emlen 1966;
MacArthur and Pianka 1966; Schoener 1971) can also be applied to plants. This thesis is plausible only insofar as plants have responses to resources that are analogous to the active behaviors of predation. The language of foraging is couched in terms of animals and their behaviors, but viewed in an operational rather than a semantic context, comparisons are possible. In this light, I have interpreted foraging responses to be responses that: (1) take place prior to resource uptake, (2) modify the probability of uptake, and (3) can be varied by
the foraging organism. An implicit premise of foraging theory is that foraging
"choicest! (investment in acquisition) are based on expected reward (Pyke et a1.
1977). Thus for a plant to "forage," it must have pre-uptake responses that can
vary adaptively in accordance with the average value of a resource. 12
The requirement for a response prior to uptake may appear to be unnecessarily restrictive: several models that fall under the aegis of foraging theory predict behavior that follows sampling of a resource, eg., movement models of nectivorous bees (Pyke 1978) or patch use models (Charnov 1976a).
However, resource uptake in these cases is a form of assessment, and is not to be confused with the results of resource acquisition. The active responses that follow evaluation of a resource are qualitative, and function directly to increase the efficiency of subsequent resource acquisition. In direct contrast to these are the quantitative and passive physiological processes of growth and survivorship that are the unavoidable consequences of uptake. These distinctions are essential in that passive, or at times programmed, growth are currently the most commonly accepted paradigms for plant resource use (e.g., Harper 1977, 1985;
Halle et aI. 1978; Bell 1984; Silvertown 1981). Because application of foraging theory to a plant is unprecedented, at least in this initial example the relationship between active response and resource use will be made clear and unequivocal
I have esamined patterns of growth and host use in the parasitic plant
Cuscuta subinclusa (dodder) to evaluate whether it uses pre-uptake responses to
increase the efficiency with which it acquires resources. Individual dodder plants
encounter many potential host individuals and species during the growing season.
Dodder possesses a potential pre.uptake mechanism. In order to obtain nutrients,
the orange, spaghetti-like stems of dodder must first coil about a host stem or
leaf before sending pegs of absorptive tissue (haustoria) into the host vascular
system (Macleod 1961). Dodder is rootless, effectively lealless, only minimally 13 photosynthetic, and totally dependent on its host. Because all of the parasite is aboveground and visible, the source of resources (i.e., the host) can be identified.
The high degree of physiological independence among the subunits (coil and subsequent stem) of dodder (C. K. Kelly unpuh. data) allows for assessment of the immediate impact of the host on the parasite through measurement of growth distal to an isolated host connection. Long-term effects of resource use can be determined from growth of an individual parasite over time.
C. subinclusa and C. costaricensis infest and grow more profusely on some host species than on others (Kelly et al. in press and unpub. data). Such patterns of host use are consistent with foraging theory, suggesting more ready acceptance of some hosts (prey or patch choice), more time spent exploiting one resource over another (patch use), changes in movement patterns in response to resources, or some combination of the above. I tested C. subinclusa for all of these potential responses. I also determined, through experiment and observation, the consequences of foraging responses for C. subinclusa, and the impact of those responses on the fitness of the parasite.
Study site
The study site, Starr Ranch Audubon Sanctuary, is a 1600 ha preserve in the foothills of the Santa Ana Mountains, Orange County, California, USA The prinCipal vegetation types are Coastal Sage Scrub (Munz and Keck 1973) in the upper reaches of the canyons and oak-sycamore riparian habitat (Thompson
1961) along the banks of the seasonal streams. In the sanctuary, Cuscuta 14 subinclusa Durand and Hilgard (Convolvulaceae) grows in both major habitats.
Average rainfall in the area is 430 mm and occurs primarily from January to
March; little to no rain falls from June to November. In recent years, the region has been swept by fire on average every 40 yr (Ascbmann and Babre 1977), although fire may been as frequent as every 8 yr in pre-Columbian times (Dodge
1972).
PREUPTAKE RESPONSE
Dodder must coil about a host before any haustoria can be formed, so that coiling necessarily precedes resource uptake. I therefore investigated the temporal relationship between cOiling and haustoria formation and the patterns
of variation in both. I asked three questions: 1) Is coiling a true pre-uptake
response, i.e., is investment in coiling determined prior to resource uptake, or is
it dependent on uptake? 2) Do coiling and number of haustoria vary among host
species? 3) Is there a cue that allows Q. subinclusa to Itrecognize" host species?
In order to answer these questions, stems of C. subinclusa were
transplanted onto individuals of Malosma laurina (Anacardiaceae), Baccharis
glutinosa (Asteraceae), Brassica cf. nigra (Brassicaceae), and Sambucus mexicana
(Caprifoliaceae), all species on which relatively large clumps of the parasite had
been found. Detached, infested host branches with live C. subinclusa growing tips
were placed in 25 mm x 200 mm test tubes that had been filled with water, 15
Figure 1. Transplant apparatus. Two parasite stems are pictured tied with synthetic yam to branches of Malosma /aurina. The stem on the left has been coiling from 12 to 24 hours and is probably still coiling. The stem on the right has not yet begun coiling. Haustoria will be initiated on the inside of the coils, where the parasite is in contact with host tissue. 16 wrapped in foil, and suspended from the branches of a target host (Figure 1).
The growing tips of the parasite were then tied to stems of the target host using red orlon yarn, insuring contact between host and parasite. The red synthetic yam also aided later relocation of the growing tip while not itself serving as a substrate for coiling. The parasites were tied to the host branches 4-S em. from the tip of the parasite stem, just behind the region of active coiling. Numbers of coils and of haustorial initials (the bumps on the parasite stem that precede formation of the penetrating haustoria) were counted for each C. subinclusa stem. on each of the following 5 days, by which time initial coiling was complete.
I also tested the hypothesis that host bark ehemicals may be a cue by which dodder recognizes a host. I obtained some of these chemicals by dipping branehes of the most heavily infested host, Malosma /Ilurina, in 80% ethanol solution. Taking care not to immerse the cut end of the branch, I dissolved only compounds present on the branch surface and with which dodder would easily come into contact. Using 2-way paper clrromatography, various groups of flavonoids were separated from one another, then individually redissolved into distilled water. These solutions were used to dip the growing tip and first 5 em of each dodder strand. The dipped detached strands were placed on a flat neutral surface of dark green polyester double-knit cloth in a 43 cm x 28 em x 6.4 em aluminum baking pan. Each pan contained 5 strands, with 2 pans for each flavonoid type and 2 pans of distilled water as a control. The pans were covered with plastic wrap to minimize evaporation, then stacked together in a 91 em x 61
em x 61 em metal traveling trunk. Number of coils was recorded for each strand 17 at three 6 hr intervals, for a total observation time of 18 hr.
Strand response to bark-wash fractions relative to that induced by distilled water alone was analyzed using repeated measures multiple analysis of variance
(MANOVA; cf. Gurevitch and Chester 1986) to determine the numbers of coils per stem per treatment.
Results
Coiling was complete by the third day after contact between parasite and host. Fifty-eight percent of the total amount of coiling observed was achieved within the initial 24 hrs, 75% by 48 hrs after contact, and from day 3 to day 5
after contact, coiling did not increase from a mean of 1.2 coils per individual
over all host species. On the other band, haustoria usually did not begin to form
externally until 24 hrs after the parasite carne into contact with a host stem; ouly
5% of the number of haustoria! initials observed on the final day were present at
the end of the first 24 hrs of contact between host and parasite. By 48 hrs after
contact, 60% of the-haustorial initials observed at the termination of the
experiment had been formed; 72% by 72 hrs and 89% by the fonrth day.
Initiation of haustoria had not leveled off by the last day of observation and
probably continued past the end of the experiment (Figure 2).
C. subinclusa can "recognize" host species and vary its response,
apparently because coiling is induced by specific chemicals in the host bark. The
final number of C. subinclusa coils and final number of haustoria initiated by the
parasite varied significantly among host species (Table 1; Figure 3). Repeated 18 measures MANOVA shows that the parasite coiled significantly more on average and more rapidly after being dipped in a solution of a group of unidentified aglycone flavonoids than after being dipped in distilled water alone (Table 1).
Discussion
The evidence reported here suggests that coiling response and investment in host exploitation do not result simply from the passive consequences of differential growth and survivorship. Instead, as required by foraging theory, parasite response occurs prior to and independently of uptake, because coiling of
C. subinclusa is complete before the haustoria become functional. When transplanted onto various host species, detached parasite stems reached maximum coiling within 72 hours. Haustoria! initiation, on the other hand, did
not begin in earnest until after 24 hours, by which time almost 60% of final
length in coil had already been achieved (Figure 2). Laboratory studies of the
sequence of haustorium formation have found that haustoria are not functional
until 4 to 5 days after initiation (Tsivion 1978). Thus, the commitment to coiling
on a host by C. subinclusa has already been completed before any host resources
are available for use in coiling. The more traditional, passive model of plant
resource use can not predict this pattern of coiling response independent of
resource uptake.
The completion of coiling by the parasite before rewards are acquired,
together with the regular differences in parasite coiling among host species,
suggest that C. subinclusa determines its coiling investment on the basis of 19
100
Z 0 ;:: 80 rr; W 2 3 [J/\ VS /\FTEn TR/\NSPL/\NT t Figure 2. Time course for parasite coiling and formation of haustoria! initials. Data pOints were derived by first determining mean number of coi1s or haustorial initials over all species for a particular day, and then calculating the percentage represented by that number of final mean number of coils or haustorial initials. The arrows at day 4 indicate the earliest possible point at which there may be functional haustoria. 20 Table 1. Summary of ANOVA, ANCOVA, and MANOVA results. Results are arranged according to questions tested. df =degrees of freedom; F = F statistic; P = probability of Type 1 error. df F P Pre.uptake response No. of coils among hosts 3,190 5.620 0.0010 No. of haustoria among hosts 3,190 3.989 0.0088 Coil induction by flavonoid relative to distilled H2O 1,20 avg 4.803 0.030 1,20 lin 4.013 0.048 Cost of coiling Elongation of coiled vs uncoiled parasite stems 1,190 172.313 <0.0001 Host value and parasite response Response and immediate reward (10 d experiment) Coiling among hosts 3,84 7.227 0.0002 Growth among hosts 3,84 6.484 0.0005 Haus/coil length among hosts 3,84 12.461 0.0046 Growth per haustorium 3,84 1.681 0.1773 Effect of change in coil length on # of haustoria among hosts 3,84 12461 <0.0001 Response and long term reward (30 d experiment) Coil length after 4 d (K) 5,115 9.225 0.0010 Rate of coiling once hegun (r) 5,115 2403 0.0410 Time to 1st coil (alpha) 5,122 1.752 0.1310 Parasite Illy wt after 30 d 5,133 5.301 0.0002 Total N content 6,18 7.667 0.000 Size and fitness Parasite survivorship relative to size (Jog transform) 1,63 10.556 0.0019 Maximum parasite size relative to genesis (log transform) 1,61 4.037 0.0489 Parasite resource status Stem thickness of parasite by fertilization trt 1,50 14.366 0.0004 Number of growing tips by fertilization trt 1,45 11.922 0.0009 Width of branched vs unbranched stems 1,61 32.379 <0.0001 Percent coiled thick vs thin stems (arcsin square root transform) 1,18 5.067 0.0371 21 ~2.5 (5 i:l100nO SAMBUCUS BACCH41US BRASSICA HOST SPECIES Figure 3. Parasite response to different host species after 5 d of contact between host and parasite. a. Mean (+ 1 S.E.) final number of parasite coils. b. Mean (+ 1 S.E.) final number of haustoriaI initials formed by the parasite. Means differ sigrtificantly in both cases (p < 0.05; Student-Newman-Kuels). 22 species-specific recognition cues. A group of aglycone flavonoid compounds that were extracted from the bark of Malosma laurina, the host species on which mean parasite length in coil was greatest, may serve this function. Although the data for flavonoid compounds in this particular role should be viewed as preliminary, other arguments strengthen the case for flavonoids as coiling cues. Flavonoids, as a group of chemicals, are both ubiquitous and specific; taxonomists use them to clarify relationships among populations and closely related species (e.g., Young 1979; Seigler 1981; Doyle 1983). Flavonoids thus are potentially able to provide a level of information useful to C. subinclusa. Flavonoid compounds exuded from the roots of the hosts of parasitic Striga sp. (Scrophulariaceae) induce haustoria to form on the roots of the parasite (Lynn et a!. 1981; Steffens et a!. 1982; Steffens et al. 1983). Flavonoids have also been implicated in the phototropic responses of plants (Sara and Galston 1968; Munoz and Butler 1975; Jesaitis et a1. 1977), such as the bending response of Selaginella (Bilderback 1984) and the coiling response of pea tendrils (Shotwell and Jaffe 1979). The connection of flavonoids with phototropic responses is especially relevant in that transplanted C. subinclusa coiled only during daylight hours (Kelly pers. obs.). Further study of the role of flavonoids in host assessment by C. subinclusa thus seems warranted, and may prove an example of plant-plant interactions mediated by secondary compounds, a phenomenon that has proven difficult to document (Harper 1977; Heisey and Delwiche 1985). In summary, I have shown that C. subinclusa possesses a pre-uptake response that varies regularly among resource types (hosts). The mechanism 23 underlying that response appears to be induction of coiling by host bark chemicals. COST OF HOST EXPLOITATION To determine if host exploitation has a cost, elongation of coiled and uncoiled parasite stems was compared. To standardize conditions among replicates, freshly cut branches of Malosma lamina were stripped of leaves and set upright in a block of white styrofoam. The styrofoam block was lighted from above by two 100 watt light bulbs approximately 1 m above the surface of the styrofoam and 0.6 m above the tips of the branches. Using cellophane tape, a 25 em lang stem of C. subinclusa was taped to each host branch below the parasite's region of coiling and elongation. The base of each parasite stem rested in a small, water-filled test tube taped to the base of the host branch. Distance from the growing tip to the tape was measured at the beginning of the experiment. Coiled and uncoiled length beyond the tape were measured after 24 hr of constant illumination. Nine replicates of 20-22 host branches with parasite stems were run over a 6 week period, June and July of 1985. Results Within the first 24 hI after contact with a host, detached parasite stems that had coiled elongated. 48% less, on average, than stems that had not coiled (Table 1; Figure 4). 24 3.5 T 2.5 .T z ~ 2 « z 01.6'" ..J W .5 UNCOILED COILED PARASITE STEM TYPE Figure 4. Cost of coiling. Mean (+ 1 S.E.) elongation of detached parasite stems that have coiled within 24 hr (N = 85) versus mean elongation of stems remaining uncoiled within the same time period eN = 85; P .5. 0.0001). 25 Discussion Even a minimal estimate of the effects of coiling on elongation shows exploitation of a host by C. subinclusa to be a costly proposition, and signifies an adaptive value for the ability to modify the coiling response relative to potential reward. Within the initial 24 hours after contact, stems elongate significantly less while coiling than they do if not coiling. Because successful exploitation of a host also includes formation of haustoria, a process which may take up to 6 dafter the conservative estimate of cost to the parasite of host infestation. The results indicate a physiological cost to coiling and also evidence of missed opportunity costs in the form of decreased probability of future contacts with other hosts. HOST VALUE AND PARASITE RESPONSE The areas of foraging which are dealt with in this section are: 1) resource choice (whether a host is infested upon encounter), and 2) variation in the relative time spent or investment made in exploiting a resource patch (the marginal value theorem or MVT). Foraging theory predicts that an item or patch is unacceptable to a forager if the net value of the resource is less than the average net intake prior to encounter (Charnov 1976b). Acceptability of an item depends only on its gross energetic value, the cost of acquiring it, or by the abundance of more valuable items. The marginal value theorem draws from the same economic model concerning marginal values to predict that a forager should remain in a patch, once chosen, until the marginal rate of capture drops to the average capture rate for the habitat as a whole (Charnov 1976a). The 26 parasite comes in contact with the host (Tsivion 1978), this measure is a time a forager should spend in a patch is determined graphicaIly as the point at which a line with a slope equal to the energy intake rate is tangent with the curve representing energy acquired over time (Figure 5). In essence, a forager wi11 spend more time in a richer patch, and in a richer habitat, wi11 spend less time in anyone patch. The accuracy of these predictions has generally been examined by observing the response of an individual to patches and resource types of different values (Krebs et aL 1983; Stephens and Krebs 1986). For dodder, however, the traditional means of comparing individual response is not available; because a coiled dodder stem does not uncoil, only one patch type can be offered to any one parasite stem. It is thus possible only to compare the responses of many dodder stems to many resources and resource types. The original statement of the marginal value theorem predicts an exact relationship between investment in and return from a resource; on the other hand, the above form. of characterizing dodder response to hosts produces a cloud of points, or an average value, for each of the two variables. Instead of being examined for deviation from a point, the data thus must be tested by another means. I would like to point out here a corollary of the original theory, which would allow a test of this particular situation. Inspection of Figure 5 shows that as the value of a patch increases, investment by a forager in a patch also increases. I therefore conclude that if dodder responds to hosts in a way consistent with the marginal value theorem, average time or investment in coiling on different host species will be correlated 27 ,1> "'-TRAVEL TIME PATCH RESIDENCE TlME_ Figure 5. The marginal value theorem. Ret) = long term average rate of energy gain. X. = encounter rate. ~ = optimal residence time. The curves represent gain functions for patches 1, 2, and 3. Optimal residence time in a patch is found by constructing a IWe tangent to the gain function and parallel to the line representing R(t), shown here as the narrow solid line. The heavy black line joins the tangent points for the 3 patches and indicates the expected relationship between energy gained and time or effort spent on harvesting a patch. In this model, search times (I/>..) are assumed to be equal among patch types and difference in gain among patch types is assumed to be only quantitative, not qualitative. 28 with the average reward from those species. The hypothesis that is being tested, then, is: On average, C. SUbulclusa invests more in those host species from which the expected reward is greatest. Host quality can be assessed in terms of the contnbution of different hosts to growth, survivorship, and reproduction of the parasite (Pyke et al. 1977). An individual dodder plant infests many hosts simultaneously and acquires more hosts as the season progresses. Thus parasite growth and fitness is not just a result of the direct interaction between one host and a parasite, but also of interactions between hosts, and of the effects of different hosts when infested in combination and over time. The role of coiling in resource uptake and the value of a host species to C. subinclusa was therefore tested both by assessing parasite success when experimentally restricted to a single host species, and by observing the relationship between dodder size and host use in the field. The relationship between haustorium formation, coiling, and host quality was determined by measuring: 1) initiation of haustoria, coiling, and growth rate of the parasite immediately following contact with the host, 2) initial coiling response and biomass accumulation of the parasite over the course of the growing season, 3) host total nitrogen content, and 4) host contribution to parasite size in nature. Immediate growth response Host-dependent coiling, haustorium formation, and growth rate of the parasite was assessed on different hosts by placing 2 detached stems directly into a 13 mm x 100 mm foil-wrapped test tube which contained water and had been 29 suspended in a target host. Each test tube contained two 3S em pataSite stems that were tied onto separate host branches, once again using red orlon yarn (Figure 1). In early July 1983, 30 stems each were transplanted in this maruier onto Malosma laurina (Anacardiaceae), Rhamnus crocea (Rhamnaceae), Artemisia californica (Asteraceae), and Lotus scoparius (Fabaceae). These species are among the four most common native perennial shrubs in the area and C. subinclusa grows on all of them. Since the potential host individuals grew intermixed within a single O.S ha site, I assumed that variation in response to host species reflected species-specific attnbutes of hosts and not atraneous edaphic factors. On the 10th day after transplanting, I measured survivorship, length of stem in coil, nnmber of haustoria, total parasite stem lengt.h, and number of branches for all parasite stems. To determine whether variation in coiling (a pre-uptake response) determines the ability of the parasite to exploit a host through its effect on haustoria formation, the relationship between coiling and number of haustoria was examined using analysis of co-variance (SPSSX, Norusis 1986). In the ANCOVA, nnmber of haustoria served as the dependent variable, length in coil as the co-variate, and host species as the nominal variable. The constancy among hosts of the relationship between haustoria number and coiling (i.e., the assnmption of homogeneity of slopes among host species) was tested by examining the interaction between length in coil and host species. Individcal regression analyses were included in the model to compare the relationship between haustoria number and length in coil for each host species. 30 Long-term growth response A third transplant experiment was performed during June to August 1985, in order to examine the effect of host identity and value on coiling and biomass accumulation of the parasite over the course of the season. Although this experiment differed methodologically from the previous experiment only in the placement of one detached stem rather than 2 in each test tube, it differed greatly in the temporal sequence of set-up and data collectioD. Parasite stems were transplanted onto Malosma Iaurina (Anacardiaceae), Brassica nigra (Brassicaceae), Eriogonum fasciculatum (polygonaceae), Lotus scoparius (Fabaceae), Sambucus mexicana (Caprifoliaceae), and Platanus racemosa (Platanaceae), using 30 stems per species. The stems were transplanted on 6 separate occasions, using 5 strands per species, at intervals of 5-7 days, so that the process encompassed not more than one hour each time. The stems were obtained from one of two parasite individuals. The order in which host species received parasite stems was rotated from one transplant event to the next in order to mitigate any effect of freshness of stem or difference in duration of contact between parasite and host in the subsequent observations of coiling. The particular host species were chosen because dodder had been found growing on each in varying degrees of infestation at least once during three years of demographic measurement, and because different degrees of acceptance by dodder had been exhibited in previous transplant experiments. The hosts represented a variety of growth forms, and differences were expected in paraSite response among host species. The growth forms are, respectively, large evergreen 31 shrub, annual (or biennial) herb, low evergreen shrub, low deciduous shrub, large deciduous tree-shrub, and deciduous tree. Of these species, only Brassica cf. nigra is not native to the study area. Based on results from the initial transplant experiment, coiling was assumed to be complete after the third day of contact between parasite and host. During the first 2 days after transplanting, number of coils was recorded every two hours during daylight hours for each stem; during the 3rd and 4th days, number of coils was noted once each day, just before dark. Length in coil was calculated from the number of coils per sample and host stem diameter, using the formula for the perimeter of a circle, since direct measurement disrupted coiling and growth. To ensure that parasite stem diameter did not affect coiling among host species, strands of as near uniform width as possible were used. The effect of strand thickness on coiling in this experiment was also tested by adding stem diameter as a co-variate to the ANOVA testing strand response to host identity. For each stem, time to first coil (alpha), rate of coiling once begun (r), and standardized length in coil at the end of the observation period (K) were calculated and compared among hosts and over transplant events. Alpha and K were extracted from the data directly. Because length in coil is cumulative, a plot of length in coil over time forms an approximate logistic curve. The non-linear regression program BMDAR (BMDP; Dixon, 1983) was used to estimate the parameter r. All resulting biomass from each transplanted stem was collected, weighed, 32 dried, and reweighed after 30 days, a period encompassing most of the growing season. In both this and the previous transplant experiments, an individual parasite stem was allowed to grow on only one host species. However, by design, the number of individuals of a host species was not constrained, so that parasite growth was not limited by availability of bost tissue. A Kjeldahl total-nitrogen assay was used to measure protein nitrogen content of the 6 host species in this experiment (cf. Feeny 1970) and of C. subinclusa. New growth and leaves-the tissue types on which parasite coils are most likely to establish (cf. Woodwell et a1. 1975)-of 3 individuals of each host species and of the parasite were collected and assayed, except for Eriogonum Jasiculatum, for which only one sample was collected. To ensure that genetically distinct individuals were sampled, tissues were collected from widely separated plants. Parasite growth in nature The last assessment of host quality was that of the observed contnbution of the above 6 host species to parasite size in nature. Individuals of C. subinclusa are largest in late July and early August. At that time I ~stimated individual size of 132 parasites as stem density times the horizontal projection of the area with that stem density, then summed that product over all stem densities for an individual. For example, a single parasite might cover 0.25 m2 with a density of 43 stems, 0.5 m2 with 18 stems, and 2.0 m2 with 1-2 (1.5) stems. The size of this parasite would then be 0.25 m2 x 43 stems + 0.5 m2 x 18 stems + 2.0 m2 x 1.5 33 stems or 22.75 m' stems. Stem density was measured by dropping a plumb-bob on a string among the parasite strands and counting the number of parasite stems with which the string came in contact. At the same time I also counted the number of individuals of each host species on which the parasite individual was growing, including only those hosts with coils and haustoria Contnbution to parasite size was estimated as the linear relationship between parasite size (log,. transform) and number of individuals of a host species. The slope of that regression was assumed to represent the growth value to C. subinclusa of a single host individual of the species in question. In this test, a single parasite individual could, and usually did, infest several host species simultaneously. This differs from the two previous experiments examining host value, in which a parasite individual infested only one host species over the course of the experiment. Immediate growth response (10 day experiment) Length in coil determined the number of haustoria that were formed. When measured after 10 d of contact between host and parasite, the exact relationship between length in coil and number of haustoria varied among host species. This is shown by the significant interaction between host identity and length in coil in an analysis of co·variance with number of haustoria as the dependent variable. However, for all 4 host species examined, number of haustoria increased with increased length in coil (Table 1; Figure 6). 34 In this experiment, length of C. subinclusa stem in coil also varied significantly among hosts, as did parasite growth (Table 1). However, C. subinclusa did not coil most on the host species on -which it grew most. A posteriori tests of differences among means in coil length and growth show that C. subinclusa coiled significantly more on Artemisia califomica than on any of the other three hosts tested in this experiment (p < 0.005; Student-Neuman-Kuels) yet average growth was greatest on Malosma laurina (p < 0.005; SNK). In contrast, a regression of mean length in coil on mean growth per haustorium on these same host species was highly significant, positive, and explained 99% of the variation in length in coil (Table 2; Figure 7a). Thus growth of the parasite was not a simple function of amount of parasite stem in coil; rather, C. subinclusa coiled more on those hosts on which, on average, it was able to grow more per haustorium within a 10 d period. On a stem-by-stem basis, stems that coil more also grow more in the first 10 d after transplant (Table 2; Figure 8). There is no comparable relationship between length in coil and growth per haustorium (Table 2). Combined with the above results, these relationships suggest that although coiling more results in more haustoria and greater growth, on average, the coiling response of C subinclusa is best predicted by expected reward, in this case efficiency of uptake. Long-term growth response (30 day experiment) Of the three parasite responses to host identity measured in the final transplant experiment, fmal length in coil (K) and rate of parasite coiling once 35 .. .. . :." .. .. NO-: Figure 6. Number of haustoria as a function of length in coil for C. subbze/usa growing on a. M. laurina, r = 0.850 (p < 0.0002; N = 25); b. L. scoparius, r = 0.795 (p = 0.0007; N = 25); c. A. califomica, r = 0.511 (p = 0.0252; N = 19); d. R. crocea, r = 0.796 (p < 0.0002; N = 14). 36 Table 2. Summary of correlation results, arranged according to qUestiOIL r = correlation coefficient; p = probability of Type 1 error; N = sample size. Host value and parasite response Response and immediate reward (10 d experimeot) Number of haustoria relative r p N to coil length Over all species 0.486 <0.0001 83 M./aurina 0.850 <0.0000 25 A. california 0.511 0.0252 14 R. crocea 0.796 0.0000 19 L. scoparius 0.795 0.0007 25 Mean length in coil relative to mean growth 0.531 0.4694 4 mean growtb/haustorium 0.994 0.0056 4 Length in coil relative to growth for ea transplant 0.387 0.0004 81 growtblbaus for ea transplant 0.057 0.6176 80 Response and long term reward (30 d experiment) Mean final coil length (K) relative mean city wt with B. nigra 0.885 0.0190 6 without B. nigra 0.859 0.0619 5 Mean rate of coiliug (r) relative to mean dry wt 0.654 0.1586 6 Mean time to 1st coil (alpha) relative to mean city wt 0.698 0.1232 6 Mean host N content relative to mean city wt 0.417 Q.4110 Length in coil relative to growth for ea transplant 0.117 0.219 112 Response and size of dodder in the field Mean fiual coil length (in 30 d expt) relative to mean increase in size per host individual with B. cf. nigra 0.069 0.8970 6 without B. cf. nigra 0.961 0.0091 5 Size increase relative to mean biomass accumulation with B. cf. nigra 0.136 0.7970 6 without B. cf. nigra 0.961 0.0221 5 Fitness Estimated seed crop relative to maximum parasite size 0.895 0.0002 8 "Inverse" seed crop relative to maximum parasite size 0.958 0.0002 Parasite resource status Stem elongation relative to width 0.870 <0.0001 43 37 .t'" I·· '!-.....,.~-".-,.:'".~-." .. YII.-."--,,,I.II".-,,..- •j' :i En !1l5 Figure 7. Relationships between parasite response and potential reward derived from the host. a. Mean (+ 1 S. E.) length in coil of the parasite as a function of mean (+ 1 S. E.) growth per haustorium on different host species (r = 0.994; P = 0.0056; N = 4). b. Mean (+ S. E.) initial length in coil per host as a function of mean (+ 1 S. E.) growth after 30 d. With the non·native B. cf. nigra included in the regression model, r = 0.885 (p = 0.019; N = 6); without B. cf. nigra, r = 0.859 (p = .0619; N = 5). c. Mean (+ 1 S. D.) initiaIlength of coil as a function of mean (+ 1 S. D.) parasite size increase per host individual infested in nature. With B. cf. nigra in the mode~ r = 0.0688 (p = 0.8970; N = 6); without B. cf. nigra, r = 0.930 (p = 0.0221; N = 5). AR = Artemisia caiifomica; MA = Malosma laurina; RH = RhamJ1us cracea; LO = Lotus scoparius; BR = Brassica cf. nigra; SA = Sambucus mexicana; .PL = Platanus racemosa; ER = EriogolZurn fasicuiatum. 38 begun (r) varied significantly among hosts, although the tbne to first coil (alpha) did not (Table 1). In addition, both the two measures of host reward, parasite biomass accumulation after 30 d and host total nitrogen content (Figure 9), also showed significant differences among species. However, initial length in coil was correlated only with average parasite dry weight on a host species (Table 2; Figure 7b). When only the 5 native host species were used to compare parasite coiling and biomass, the model did not differ significantly in its explanatory power (Table 2). suggesting that the parasite did not differ in its response relative to this measure of potential reward for native and non-native species. Cause and effect of coiling and biomass accumulation is not established by this regression alone, however. It might be that, rather, C. subinclusa only accumulated more tissue because it coiled more. If this were so, then coiling of an individual stem should be a better predictor of biomass accumulation over the season, and this was not the case (Table 2). I therefore conclude that C. subinc/usa invests in coiling based on, and in proportion to, expected long-term reward. No significant relationship existed between either rate of coiling or time to first coil and average parasite biomass accumulation, or between final length in coil, rate of coiling or time to first coil and host nitrogen content. Average host nitrogen content a1so did not predict average parasite dry weight after 30 d (Table 2). 39 .8 E 38 .3 Z o ;: « ~ 24 o ..J W ::;; W ~ 12 I o I I 12321211 33 121 2 13 2 6 12 18 2. LENGTH IN COIL AFTER 10 D Figure 8. Growth after 10 days as a function of length of parasite stem in coil, for all transplants pooled over all host species (r = 0.3867; P = 0.0004; N = 81). Numbers represent number of identical data points. 40 I- Z 1.' I- "'Z 0 0 Z "'0 II:'" r=- t: Z r-- .5 MA BR SA PL LO ER cu SPECIES Figure 9. Mean nitrogen content of hosts and parasite C± 1 S.E.). CU = CUsclita subinclusa. See Figure 7 for key to host species. 41 Parasite growth in nature The increase in parasite size due to infesting an individual of a particular host species varied among the 6 host species examined (p < 0.05; Figure 7c). However, exploitation of a host species by C. subinclusa is not necessarily independent of parasite use of other species. In particular, increases in number of Malosma lawina used were frequently accompanied by increases in number of Lotus scoparius exploited (F3,28 = 3.60; P = 0.0262). Nonetheless, when only native species are considered, the average increase in parasite size due to infestation of a host individual explains 92% of the variation in initial coiling of parasite stems (Table 2; Figure 7c). There is a potential bias in this test. Host species that are rare in the habitat may be more likely to be infested by large parasites and the larger the parasite, the more individuals of that rare species it is likely to infest, just by chance alone. If this were the case, however, one would expect a negative association between number of parasites infesting a particular species and the slope of size on number of individuals. No such negative relationship exists, suggesting that the measure reflects a biological relationship rather than just a sampling phenomenon. In summary, then, initial coiling of C. subinclusa on a host was in proportion to average size increase derived from infesting that species in nature. It is notable that when the non-native host species, Brassica cf. nigra, was included in the regression model, the relationship between increase in parasite size and average length of parasite stem in coil was no longer significant (Table 2). 42 For the native host species, the majority of size increase in the field is accounted for by the interaction between the parasite and that host. Without B. ef. nigra, parasite dry weight accumulation explains 84% of the variation in size increase in nature; with B. cf. nigra, it explained less than 2% of the variation in parasite size in the field and was very clearly not a significant relationship (Table 2; Figure 10). Host choice All hosts species were acceptable to C. subinclusa in this study, that is, C. subinclusa coiled readily on all the species onto which it was transplanted in the des enbed experiments. A possible explanation could be that plants can only accept a resource, and therefore choice models are not applicable to plants. However, I have observed dodder "reject" hosts: transplanted stems of dodder will grow at right angles to a host branch rather than coil about it. Rather than not being applicable, I believe foraging theory actually offers an explanation for the pervasive acceptability of hosts to dodder at the time of the reported transplant experiments. In models of foraging, net resource value is calcul:.'.ted as E Th+ Ts where E = the energy gain from a resource, T h = the cost of handling the resource, once captured, and Ts = the cost of searching. In animals, costs 43 .25 «--' :> g 0 .15 ~'" 1- '"0 J: .05 LO 0:u, PL a. w ER «'" (JJ -.05 a: <.) ~ LU N en -.15 «Z W :;;; BR -.25 0 .25 .5 .75 1.25 1.5 1.75 MEAN DRY WEIGHT AFTER 30 d Figure 10. Relationship of mean (+ 1 S. D.) size increase of C. subillclusa in nature per host individual to mean (+ 1 S. D.) dry weight accumulation of the parasite on that species. See Figure 7 for key to species abbreviations. When only native species are considered r = 0.9146 (p = 0.0296; N = 5); when the non-native B. cf. nigra is also included in the regression r = 0.1362 (p = 0.7970; N ~ 6). 44 generally are measured as time, hence the use of T to represent costs. In plants, the costs may be of time, but also of growing entirely new structures in order to come in contact with and exploit a resource. I suggest that search and handling costs for C subinclusa at the time of the descn"bed experiments were so great that they dominated the evaluation of host quality. I offer the following evidence in support of this conclusion. The tests of host quality descnbed in this paper all took place in July and August, during the driest season in the chaparral (Miller and Poole 1979). Plant growth at this time is relatively more costly than earlier in the season, when water is more easily obtained (cf. Bloom et aI. 1985). In a transplant experiment conducted during the rainy season in early April of 1984, 19 out of 27 parasite stems grew away from the P. racemosa stems onto which they had been tied, 3 grew parallel to the host branch but did not COll, and only 5 of the 27 actually coiled about the host within 3 days of observation. In contrast, of 28 parasite stems transplanted onto M. laurina at the same time, only 2 grew away from the host, 5 grew parallel, and 21 coiled about a host stem or leaf petiole. I interpret this "rejection" of a less profitable host (P. racemosa vs M. laurina) to be a result of lowered search and handling costs due to greater water availability, so that between·host differences in energetic value would have a relatively larger impact on the evaluation of host. quality. Results of another transplant experiment suggest that differences in host value, when exceptionally large, may override even the high growth costs of the dry season. During July 1984, parasite stems were transplanted onto freshly cut branches of M. laurina and onto branches of this species that had been cut and 45 allowed to dry for 2 months previously. All of the 24 stems on fresh host branches coiled within the 7 day experiment. In contrast, of the 24 parasite stems transplanted onto dried branches, only 5 had coiled by the last day of observation. C. subinclusa may not respond to dead tissue because it does not receive appropriate coiling cues. Nonetheless, the effect is the same as a more subtle assessment: an unrewarding host is rejected. "Whether less extreme differences in host quality can also lead to rejection is still an open, but testable, question. Coiling and uptake Investment in resource acquisition by C. subinclusa affects its probability of return: the length of parasite stem coiled about a host detemiines the number of haustoria that are formed and thus the amount of resources the parasite can acquire from a host (Table 2; Figure 6). Host quality and patch use Because coiling entails a physiological cost, processes that promote appropriate investment in hosts might be expected. As foraging theory predicts, C. subinclusa coils more on those host species on which, on average, it 1) grows more stem per haustorium, 2) accumulates more biomass over the course of the growing season, and 3) gains more size per host individual when growing in a natural situation on many host species (Figure 7). Investment in resource acquisition by C. subbzclusa is consistent with expectations based on the marginal 46 value th~rem: the parasite invests in a host (i.e., a resource patch) in proportion to the value of that host species to the parasite (Charnov 1976a; Figure 5). Initial coiling respoose in C subinclusa is gauged to average uptake per haustorium when growth is measured 10 days after contact between host and parasite (Figaro 7a). Thus, in the short-term, investment in eoiling by the parasite is correlated with efficiency rather than maximization of uptake. This response appears to be advantageous in that length in coil is correlated with number of haustoria (Figaro 6) and growth on a stem-by-stem basis (Figare 8). C. subinclusa coils most on those host species on which, on average, it accumulates the greatest amount of tissue within 30 d after contact. When Co subinclusa is restricted to a single host species, average length of parasite stem in coil is most closely correlated with mean biomass accumulation of the parasite (Figore 7b). 'This relationship is not merely a result of plants that coil more managing to grow more. The lack of correspondence on a stem·by-stem basis between initial length in coil and this measure of host value, over the course of the season, shows that biomass accumulation is not a simple function of coiling (Table 2). The conclusion indicated by these data is that: 1) dodder coils in proportion to expected reward, and 2) over the course of the growing season, the short-term effects of coiling response may be overridden by other factors. The explanatory power of the regression model for long-term biomass accumulation as a function of initial coiling response does not differ greatly whether or not the introduced species Brassica cf. nigra is included in the 47 regression (73% of the variation in colling is explained without B. nigra versus 78% with all 6 host species). However, C. subinclusa's coiling response is more closely correlated with the size attained over a growing season by naturally occurring, unmanipulated parasites using different hosts, wbich accounts for 92% of the variation among hosts in length of C. subinclusa in coil (Figure 7c). Interestingly, in the latter case parasite growth effectively explains parasite coiling response only when the non-native B. nigra is excluded from the model. Mean nitrogen content of a host species predicts neither average parasite growth nor coiling response, contrary to that expected if host use by C. subinclusa is analogous to insect phloem feeding (sensu Atsatt 1977). In several species of aphid, seasonal changes in use of host species are positively associated with host nitrogen levels or with leaf conditions associated with high levels of available nitrogen (Kennedy et al. 1950; Dixon 1970, 1985). However, contradictory expectations are aroused by the observation that the aphid Tuberolachnus salignis increases its feeding rate with decreased host nitrogen content (Mittler 1958). Regardless of the particular behavior chosen as a model, insect phloem feeders seem to be sensitive to host nitrogen levels, more so than are leaf-chewing insects (Ught!oot and Whitford 1987)_ There is not the disparity in nitrogen content between C. subillclusa and its hosts (Figure 9) that there is between an insect herbivore and its plant hosts (Mattson 1980) and dodder does not respond to interspeCific differences in host nitrogen. However, C. subinclusa responds to fertilized host with increased parasite growth and branching, suggesting that C. subinclusa is affected by intra-specific host nitrogen levels. 48 FITNESS A measure of size is only important in terms of fitness to the extent that it predicts parasite survivorship and reproduction in nature. To test the relationship between size and fitness, I followed 150 individuals of C subinclusa through more than 2 complete cycles of parasite establishment, growth, reproduction, and over wintering. At 1 to 1.5 month intervals, parasite size and host use were recorded as descnbed above. To determine whether larger parasites are more likely to survive, I compared mean maximum size of parasite individuals that survived to the beghming of the next growing season (March of the following year) with those that did Dot. The effect of over-wintering on subsequent size was measured by comparing maximum size just prior to flowering of individuals to that started the season with dried parasite tissue from the previous year, to those without it. A regression of size of seed crop on maximum parasite size prior to reproduction was used to estimate the relationship between parasite fecundity and growth in nature. Seed-crop size of 8 parasites was assessed after fruit set was completed at the end of the previously descnbed demographic survey. Seed set of C. subinclusa tissue growing on M. lauriJw is extremely prolific both because of number of parasite seeds set per em of infested host stem and because of the large amount of M. /aurina stem usually infested by parasites. Therefore I estimated number of seeds from parasite tissue on M. laurina by multiplying length of host stem with seed-bearing parasite tissue by average number of seeds set by C. subuzclusa per em infested M. laurina stem. Average number of seeds/em from parasite tissue growing on M. lawina was obtained by 49 counting parasite seeds per em of M. /aurina stem for 20 infested individuals. When individual dodder plants infested additioual host species, the number of seeds from those hosts was counted directly, then added to the estimated seed set of parasite tissue growing on M. laurina. Maximum parasite size during the preceding season was obtained from the demographic survey. Fecundity/per unit body mass sometimes varies with organism size (NikoJsky 1963; Abrahamson and Gadgil1973; Hickman 1975; Garwood and Horvitz 1985), and the assumption of an equal number of seeds set/em host tissue for all plants regard1ess of size may not be appropriate. If seed se!/unit plant mass varies positively with plaot size in C subinclusa as it does in many other plants (Harper 19n; Samson and Werk 1986; SiJvertown 1987), then there is an even greater reproductive advantage to large size than is indicated by the positive regression above. If seed set/unit plant mass varies inversely with plant size (Kawano and Masuda 1980) then a positive relationship between plant size and fitness may not exist. I tested this hypothesis by assuming that parasite seed set/em stem of infested host varied inversely with total amount of seed~bearing tissue, the upper and lower ranges of seed set being defined by the 95% c.r. about the mean of seed set/em of infested stem of M. laurbUl. Resu1ts Both survivorship and reproduction of C subinclusa depend on parasite size. Large parasites were more likely to successfully survive the end·of·season drought and over·winter vegetatively, thus growing and setting seed an additional 50 year (Table 1; Figure 11a). Parasites occasionally over-wintered successfully without leaving any obvious dried tissue from the previous season. Thus some individuals that actually over-wintered may have been falsely assumed to have arisen from seed that season, inappropriately increasing the mean size of that group. Nonetheless, average size of parasites assumed to have originated from seed was significantly less than that of clearly over-wintered parasites (Table 1; Figure llb). Large parasites made more seed-bearing tissue and seeds (Table 2; Figure lIe). If it is assumed that each em of M. laurina stem with seed-bearing C subinclusa tissue produced the average number of seeds/em found on M. laurina stems, then there was a strong positive relationship between parasite size and fecundity. The uinverse estimate" of seed crop size also resulted in a positive regression of parasite seed crop on size. Thus even if larger parasites should produce fewer seeds per crn of host stem infested, greater parasite size would still lend a significant fitness advantage in terms of total seed set (Table 2; Figure Ud). Discussion Both survivorship and fecundity were positively correlated with parasite size. Larger parasites were more likely to survive the end-of-season drought and set seed a second year (Figure 11a). Those parasites that successfully over wintered were, on average, larger just prior to flowering than those that had 51 .. ..."XIMUI.I PARASITE SIZE Figure 11. Parasite size and fitness. a. Mean (+ 1 S.E.) size in August 1982 of parasites that successfully over-wintered to the 1983 growing season (N = 17) versus those that died during the fall or winter (N = 47; loglO transform of parasite size; p = 0.0019) b. Mean (+ 1 S.E.) maximum size of parasites arising that season from over-wintered tissue (N = 36) versus that of individuals assumed to have arisen from seed (N = 27; loglO transform of parasite size; p = 0.0489). c. Estimated seed crop as a function of size of parasite just prior to flowering (loglO transform of size; r = 0.895; P = 0.0002; N = 8). Seed crop is estimated as em of infested host tissue X average number of parasite seeds set per em of infested M. laurina, the host upon which C. subinclusa sets the vast majority of its seeds, plus numbers of s~ed set on other host species (see text). d. Estimated seed set per as a function of parasite size when it is assumed that larger parasites set fewer seeds per em infested host branch than smaller parasites (lOglO transform of parasite size; r = 0.95757; P = 0.002; N = 8). The range of seeds set per cm infested host tissue was taken as the 95% c.l. about the mean of seeds set per em of infested M. lamina. 52 started from seed that year, compounding the advantage of increased survivorship due to size (Figure llb). Those parasites that reached greater maximum size, regardless of starting that season from seed or over-wintered vegetative tissue, resulted in more host stem covered with seed-bearing tissue and thus produce more seeds (Figure llc and d). In summary, the coiling response of C subinclusa, its ''foraging behavior", is positively connected to fitness through its relationship with increased parasite size. I believe it is worth noting here that only one other study has successfully made this connection between foraging response and limess (Whitham 1978). PARASITE STATUS AND COILING In animals, resource status as well as perceived prey value has been postulated to affect the degree to which a predator will discriminate among prey. In other words, a hungrier predator is more willing to invest, or willing to invest more, in less valuable prey (e.g., Sibley and MacFarland 1976; Charnov 1976b). Because a parasite stem has no leaves or other potential storage organs, nutritional status, or hunger, should be reflected in stem diameter. The relationship of diameter to several factors affecting parasite success was investigated so that the effect of nutritional status on coiling could be examined. The effect of stem thickness on growth was determined by measuring elongation of parasite stems of various diameters. Stem diameter was measured 2S em behind the growing tips of 30 parasite stems and each stem was marked 2 em behind the tip with a small dot of black waterproof ink. After 24 hr the length of 53 stem beyond the ink mark was recorded. The accuracy of stem diameter as an indicator of parasite nutrient status was further tested by comparing the width and number of stems of C. subinclusa growing on fertilized and unfertilized individuals of Malosma /aurina growing in pots. For the enriched treatments, individuals hosts were fertilized with slow release pellets of 18-7-10.NPK compound (Sierra blend) as well as watered twice a week for 4 weeks with a weak solution of 18-0-0 NPK (Osmocote). Both treated and untreated host individuals were watered once a day, the total amount of fluid adjusted so that it was the same for both treatments. Two weeks after the fertilization treatment began, a single stem of C subinclusa from one of two parent parasites was transplanted onto a host individual and allowed to grow there for 7 days before measurement. All stems arising from an established coil were counted for each of the 18 host individuals; the diameters of 45 of these stems were measured at the stem base. The relationship between stem width and branching was also examined non-experimentally. The width 25 em behind the growing tip was compared for unbranched parasite stems and stems branched within 10 em of the tip, all of which were growing on M. laurina. The effect of parasite resource status and resource recognition upon coiling response, i.e., prey pursuit, was documented using an experimental set-up slmilar to that used for the previously descnbed test of host bark chemicals and coiling response. Detached parasite stems were divided into two size groups: thin « 0.09 mm) and thick (> 1.1 mm). Stems from each size group were dipped in a 54 mixture of one of 9 known flavonoid solutions or distilled water. Ten stems were used for each chemical treatment, 5 thin stems to one pan and 5 thick stems to a second pan, totalling 100 stems for the experiment. Coiling response again was observed every 6 hr for 18 hr and analyzed for percent of strands coiling given the 2 factors of width and flavonoid type, using 2-way analysis of variance (SPSSX, Norusis 1986). Total percent of stems coiling relative to stem width was also examined. Results Parasite stem diameter appeared to be a good measure of parasite resource status. The thicker the stem initially, the more rapidly it elongated (Table 2; Figure 12a). Parasite stems growing from coils on fertilized hosts were thicker than stems growing from coils on unfertilized host individuals (Table 1; Figure 12b). Stem branching in the parasite was also associated with resource status. Coils of transplanted C. subinclusa stems on fertilized hosts developed more growing tips than did parasite stems on unfertilized hosts (Table 1; Figure 12c). Not surprisingly then, branched stems on naturally occurring parasites were significantly thicker than unbranched stems (Table 1; Figure 12d). Resource status, as measured by stem thickness in C. subinclusa, affected parasite response to a host. Thin parasite stems were more likely to coil than were thick stems and had more coils per stem than thick stems (Table 1; Figure 13). Although number of coils per stem also varied among flavonoid treatments, response to flavonoids did not vary between the thin and thick stems (Table 1). 55 --~ Figure 12. Parasite stem width and nutritional status. a. Elongation over 24 hr of C. subinclusa stems as a function of initial parasite stem width measured 25 em behind the growing tip (r = 0.8703; P < 0.0002; N = 43). b. Mean (+ I S.E.) parasite stem width 25 cm behind the growing tip of branched (N = 31) and unbranched (N = 30) stems (p < 0.0001). c. Mean (+ I S.E.) parasite stem width of parasites growing on fertilized (N = 33) and unfertilized (N = 17 individuals of M. laurina (p = 0.0004). d. Mean (+ I S.e.) number of branches per coil of parasites growing on fertilized (N = 42) and unfertilized (N = 31) individuals of M. lawina (p = 0.0009). 56 Discussion That thin and thick parasite stems possess different growth patterns affects the ability of the parasite to exploit hosts in several ways. In C. subinclusa, branching is positively correlated with both parasite stem thickness and nutrient status of the host (Figures 12c and d). Branching creates more meristems, the site of active coiling, and can enhance the ability of the parasite to exploit a host. Analogous to the increased turning response of bees after location of a nectar source (Pyke 1978), this propensity to branch in C. subinclusa enables the foraging individual to exploit efficiently a patchy resource. Although a passive model of plant resource use would expect greater growth in response to resource acquisition, it would not necessarily predict the qualitative change in branching, providing another instance where foraging models constructed to descnoe animal behavior would be useful in understanding plant responses. A demonstrated cause of variation in parasite coiling response is that thinner, more resource-poor stems of C. subtizelusa were more likely to coil, and coil more, than thicker, more resource-rich stems (Figure 13). Pulliam (1974) originally predicted that resource value alone determines the investment by the predator in resource acquisition. Charnov (1976b) and Sibley and McFarland (1976) were among the first to postulate that predator resource status, "hunger", also affects investment in acquisition. Coiling response in C. subinclusa is consistent with the predictions of the latter models, and in accord with current thought on the effect of the state of the predator in foraging decisions (e.g., Mangel and Clark 1986). 57 100 o '"z I_._._·1I THIN STRANDS ., 80 ....0: ..· ..· .. r o'" f ~ 60 o tr'~·~~~ "1z 40 W "ffi 1 Q. I. HOURS AFTER TREATMENT 1.6 T 01~ ~ o 1 T Ii" w 8 0: "W Q. 6 4 0 THIN STEMS WIDTH GROUP Figure 13. Parasite stem width and coiling response. a. Time course of coiling response of detached parasite stems. b. Mean (+ 1 S.E.) percent coiled of thin parasite sterns « O.09mm; N = 10) and thick parasite stems (> 0.10; P = 0.0371; N ~ 10). 58 GENERAL DISCUSSION In plants, resource use is inextricably bound to plant growth. Darwin (1875, 1881) recognized that plant growth responses could result in a fit between resource requirements and individual distribution. More recently, it has been suggested that growth patterns in clonal plants may be a form of habitat selection (penalosa 1978; Cook 1983, 1985; Salzman 1985). Salzman (1985) has suggested that plants· may also actively select one environmental regime over another, rather then merely responding passively to the consequences of differential growth and survivorship. Not surprisingly, then, the active tenn "foragingu recently has been borrowed from animal ecology to describe potentially adaptive plant growth patterns (Bell 1984; Slade and Hutchings 1987a, b, and c). The metaphor was coined in order to empbasize that growth patterns affect resource acquisition in plants in a manner analogous to behavior in animals (Bell 1984). However, I propose that the comparison may extend beyond analogy or metaphor, so that the well-developed body of theory on animal foraging can be used to better investigate the rewards and constraints underlying plant growth and resource use. That foraging models have been couched in the vocabulary of animal behavior may have obscured their potential generality. Stripped of taxonomic association, the purpose of foraging theory is to predict the pre-uptake responses of an organism to a resource. The working hypothesis of foraging theory, and the assumption against which results are tested, is that the response of an organism to a resource depends on the expected reward, and is not the direct result of 59 resource uptake (Pyke et al.1977; Charnov 1976a and b). Such active responses alter the probability of resource acquisition, in contrast to differential growth and survival, which are the passive aftermath of resource uptake (Schoener 1971; Pyke et al. 1977; Krebs 1978; Krebs et al. 1983; Pyke 1984; Stephens and Krebs 1986 provide reviews of foraging theory). Adaptation That C. subinclusa responds adaptively to the native hosts but not to the one non-native species supports the idea that parasite coiling response is the result of natural selection. Examination of the subsection Subinc1usae of the genus Cuscuta shows that species of Cuscuta closely related to C. subinclusa do not use the same or even closely related host species (Yuncker 1932). Nor does C. subinclusa necessarily infest species related to the hosts on which it coils. Although frequently in contact with it, C. subinclusa does not infest Rhus diversiloba (poison oak), a member of the same family as Malosma laurina, the species on which the parasite both coils and grows most. These two lines of evidence suggest that patterns of host use in C. subinclusa may not be constrained by phylogenetic history, probably because effects of host taxonomy are overridden by strong selection to select hosts on the basis of their contributions to growth. However, note the disparity between the ability of C. subinclusa to accumulate biomass on Lotus scoparius when restricted to this host species (Figure 7a) and the apparent contribution by L. scoparius to the parasite in the 60 field (Figure 7c). I suggest infestation of this host species to be an advantage through its service as a "bridge" between individuals of host species on which C. subinclusa is able directly to accumulate greater biomass. Thus value of a host species to the parasite appears not to be a process of simple differential growth and survival on the various host species used by the parasite (cf. Wint 1984). Although complexity of interactions or structures does not prove past selection for the current purposes they serve, combined with the above phylogenetic evidence, I believe that we can infer strongly that the pattern of host use in C subinclusa reflects adaptation as well as adaptiveness (cf. Sober 1985). Variation in coiling response The coiling response of a C. subinclusa individual is highly variable, both within and among host species (Figure 7). I believe this pattern reflects the sensitivity of C. subinclusa to factors other than host identity alone and can be attnbuted to the need for the parasite to remain behaviorally fleXIble in an environment that changes on several time-scales as wen as in space. From season to season, water status and consequent physiological activity of host species can vary substantially (Poole and Miller 1975; Miller and Poole 1979). Because of the frequent fires in this habitat, vegetation composition and physiognomy, in addition to plant physiology, can change drastically from one year to the next, well within the lifetime of a C. subinclusa individual, which I have so far found to be as long as five years. Therefore I suggest that variability in the environment puts a limit on parasite specialization, and the canalization of coiling responses. 61 Conclusions Although passive growth responses by C. mbinclusa could have explained some of the observed patterns of host use by the parasite, the use of a model of active choice in this case provided a heuristic tool that revealed additional causes for differences among hosts in parasite infestation, causes that otherwise would have been unsuspected. For example, a passive growth model would not predict the relationship between differences in C. subinclusa coiling response and the value to the parasite of host species, the role of host bark chemicals in parasite coiling, or the qualitative change in growth represented by the onset of adventitious branching in response to resource enrichment. The application of foraging theol}' has proven useful in understanding the ecology and patterns of growth of C. subinclusa. Evidence suggests that plant "foraging" may be more widespread than in just this one admittedly atypical and highly specialized genus of plants. Responses that might fit into a foraging context have been observed in other, independently evolved, parasitic plants. For example, the genus Cassytha, in the Lauraceae, is amazingly like Cuscuta. The morphology of a mature plant is virtually indistinguishable from that of dodder, and the patterns of host use may also be similar (Kuijt 1969). In Orthocarpus pwpurascens the presence of cellulose fiber induces root proliferation (Atsatt et aJ. 1978). O. purpurascens is a root parasite and may be using this indicator of host presence to signal that a payoff for this action is reasonably certain. Autotrophic plants are also able to respond to changes in resource availability, as is required of a forager, through qualitative and quantitative 62 changes in growth. Lateral buds of Agropyrum repens will break dormancy in the presence of high nitrogen levels (Wareing 1964)? thus taking advantage of patchy nutrient availability. Salzman (1985) suggests that uptake~independent responses may occur in the use of saline habitats by the autotrophic plant Ambrosia psilostachya, resulting in a match between habitat and genotype. Examples of morphological switching in clonal plants (Penalosa 1983; Lovett Doust 1981a and b, 1987; Slade and Hutchins 1987a, b, and c) also support my thesis. Under resource poor conditions such as low light or nutrient regimes. many plants undergo "etiolationtl: increased internode length, decreased branching or [arnet development, and smaller, shorter-lived leaves (penalosa 1978; Noble and Marshall 1983; Slade and Hutchings 1987a). In these cases, a single individual is capable of both etiolated or normal growth. As pointed out by both Nobel and Marshall (1983) and by Slade and Hutchings (1987a), the effect of these changes in architecture could be to minimize tenure in resource~poor areas and to increase time spent in richer areas. I cite these studies because the described responses seem to be qualitative changes based on potential or expected reward that can increase the probability of resource acquisition, i.e., encounter with resource-rich habitats. These examples have in common the reallocation of currently held resources in order to increase the probability of future resource uptake. Conceivably this is possible in any plant, parasitic or not, clonal or not. If these are true non-passive responses to resource change, then the economic models of foraging theories could be used to predict the likelihood and extent of morphological response that might be 63 expected given the level of change in nutrient availability. The study of resource use by C subinclusa has relevance to the study of resource acquisition in general. That thin, resource-poor parasite stems more readily respond to the presence of resources than resource-rich stems offers strong support for the hypothesis that the resource state of foraging organisms and not just the value of the resource alone alter responses to resources. However, the '!foraging" of C subinclusa, and potentially of other plants, has other implications for those studying resource acquisition in nature. Plants, particularly clonal plants, have their patterns of past resource use, their "foraging decisions", etched in their architecture. Resource uptake in plants is usually expended in growth of one sort or another, rather than in extensive movement as in most animals. The record of foraging history and its consequences are simultaneously available for analysis. Students of issues in sexual selection have already taken advantage of the substitution by plants of structure for movement, and have found that plants can provide data not readily available through the study of animals (see reviews by Charnov 1982; Willson 1983; Willson and Burley 1983). I suggest that plants may provide a similar source of desirable study organisms for some of the questions of resource acquisition raised by foraging theory, and in the process benefit researchers in both plant and animal sciences. 64 CHAPTER TWO Population level patterns of host use by Cuscuta subinclusa: Host abundance and spatial array INTRODUCTION Cuscuta subinclusa (Convolvulaceae), commonly known as dodder, is a parasitic plant that infests hosts by coiling about the host stem or leaf, after which the parasite sends pegs of absorptive tissue (haustoria) into the host vascular system. Individual stems of C subinclusa respond to hosts in a way predicted by foraging theory in that a stem coils on (invests in acquiring) a host in proportion to the potential reward from that species (Chap. 1). Length in coil is analogous to time spent in a patch by a foraging animal (sensu Charnov 1976a), and is highly correlated with host quality. Because it seems to attack all species with which it comes in contact, and can grow on many host species, it has been assumed to be a non-discriminating generalist (Dean 1934, 1935; Gaertner 1950; Baldev 1962; Hassawy 1973; Ashton and Santana 1976). My work has clearly shown this to be incorrect, and that dodder discriminates among hosts. Thus, for C. subinclusa, individual level adaptations cannot necessarily be inferred from population level patterns. Here I ask the reciprocal question, can population level patterns necessarily be predicted from a det'ailed knowledge of individual traits? In the study described in this paper, I address this question by answering the more specific question: What factors predict the diet of a non-monophagous parasite 65 or herbivore? C subinclusa responds to hosts in a way predicted by foraging theory, but also infests plants and uses resources at the same scale as many invertebrate herbivores. Therefore I draw upon current theories of resomce use by foraging animals and by insect herbivores to construct a series of hypotheses concerning resource use by C subinclusa. I hypothesize that resource use by C subinclusa is determined hy 1) individual level response to hosts, 2) descriptors of the habitat, or 3) interaction between the above two factors. Each hypothesis offers specific testable predictions, which I present below. Individual response. I have shown that, on average, individual stems of C subinclusa coil more on more rewarding hosts (Chap. 1). Although length in coil is correlated with subsequent growth, coiling is complete prior to resource uptake. Thus initial coiling response is an active mechanism that determines resource acquisition, in contrast to a passive result of resource uptake. However, average length in coil is better predicted by expected, or average, reward than by actual reward, signifying that dodder is responding to general characteristics of the host, as might a foraging animal. If this ''foraging response!! determines population level patterns of host use, then dodder individuals should aggregate on those host species on which it coils most, as foraging animals are expected to aggregate in more desirable patches (cf. Hassell and May 1985). The first prediction to be tested is that C. subinclusa will be more common on host species for which it has a greater coiling response. Dodder ex1nbits a greater rate of biomass accumulation on some host species than others (Chap.1). Biomass accumulation reflects parasite fitness since 66 there is a positive correlation of parasite size with seed set. Thus there is selection for dodder to infest those hosts on which it is ab!~ to grow larger. The model of Fretwell (1972) would suggest that in this situation, dodder will use less rewarding hosts only when the more rewarding hosts have been depleted to the point where the return from either one is equal. This has been shown to be the pattern of host use for Pemphigus aphids, another phloem-feeding herbivore (Whitham 1978). This predicts the ideal-free distnbution among habitats of consumers (Fretwell 1972), and that less rewarding host species should not be used before a more rewarding host species has been infested. Prey choice models (Schoener 1971; Charnov and Orian, 1973; Emlen 1973; Maynard Smith 1974; Pulliam 1974; Werner and Hall 1974; Charnov 1976h) can be developed to construct a similar although not identical pattern of host use at the population level. Prey choice or diet models predict that less valuable resource types are used only if more valuable resources do not meet energy requirements. If this rule determines host use by dodder, then those host species on which dodder accumulates more biomass should be completely infested before any of the species on which dodder grows less rapidly are attacked. Habitat traits. Two more predictions are generated by the hypothesis that host use in C. subinclusa is determined by the probability of encounter between host and parasite. Atsatt (1977) pointed out the analogy between herbivorous insects and parasitic plants: both groups suffer similar problems with desiccation and host location. The analogy is particularly easy to see with C. subinclusa. As with a generalist insect herbivore, C. subinclusa 1) makes many contacts with 67 hosts over its lifetime, 2) has a range of hosts that are acceptable (can be infested) but differ in suitability (sensu Southwood 1962; Barbosa and Greenblatt 1979; Lance 1983), and 3) uses host chemicals to "recognize" hosts (Chap. 1). Herbivorous insects with a range of diet similar to that of dodder use more abundant host species more frequently (Singer 1983; Rowell 1985), apparently through increased probability of encounter. If probability of encounter with acceptable hosts determines host use, then C. subinclusa will infest hosts in proportion to the frequency of the species in the habitat. The final prediction is based upon constraints on host use specific to C. subinclusa. Malosma laurina (Anacardiaceae) is a sustaining host (sensu Krohn 1934; Atsatt 1983) for C. subinclusa, essential to C. subinclusa's survival in the habitat. In this population, greater than 99% of parasite seeds are set on M. laurina (Chap. 1). Seeds germinate either on the host or on the ground immediately beneath the host. Successful establishment of the parasite requires initial infestation of M. laurina. C. subuzclusa also successfully over~winters only on this host species. Thus, infestation of any and all host species is preceded by initial infestation of M. laurina. If origination from M.lawina determines host use, then infestation of a host species will be determined by the proximity of that species to M. laurina. Interaction. Because resource use is a complex phenomenon, all of the above factors will be tested in combination as well as singly. 68 MATERIALS AND METHODS Study site and study organism The study site, Bell Creek Canyon, is 17 km inland from San Juan Capistrano in Orange Co., CA The canyon runs NoS, forming the principal drainage route for Starr Ranch Audubon Sanctuary, a 1600 ha reserve in the foothills of the Santa Ana Mountains. Coastal sage scrub (Munz and Keck 1973) predominates on the sides of Bell Creek canyon, with oak-sycamore riparian vegetation in the hottom of the canyon along the vernal stream. Annual rainfall is approsimately 430 mm and falls primarily between December and March. A mediterranean clhnate characterizes the area (see Miller et al. 1978 for a detailed clhnate description). In recent years, the region has been swept by fire approximately every 40 yr (Aschmann and Bahre 1978), although it may have been as frequently as every 8 yr in pre-Columbian times (Dodge 1972). The study organism, Cuscuta subinclusa Durand and Hilgard (ConvolvuIaceae), has no roots, essentially no leaves, and is at best only minimally photosynthetic. The orange or yellow spaghetti-like body of the parasite is totally aboveground, and all host-parasite connections' can be identified and measured. Dodder seeds germinate from November to early March in response to rainfall. Vegetative growth begins in March and April, either from germinating seeds or from small bits of vegetative tissue that survived from the previous growing season. C subinclusa continues to grow and infest additional hosts until August or September, with a peak in host use during late July through 69 mid-August. Prior to the onset of flowering in late August, parasites die back to tissue closely appressed to the host stem, there forming the flowers and setting seed. Figure 14 illustrates C. subinclusa's phenology. Host use I characterized host use by C. subinclusa during August 1982 by identifying and counting all hosts infested by 67 parasites, and calculating mean number of host individuals used per parasite for all 8 host species for which coiling response was known. If any of the 8 host species was not encountered by an individual parasite, use was set equal to 0 in the calculation in order to account for the frequency of encounter with potential hosts as well as number of individuals infested when encountered. Mean number of host individuals per parasite was then multiplied by an estimate of host size (area of the canopy), for a measure of host use in terms of host area covered with parasite. Parasite response to host species In a previous study, coiling response of C. subinclusa to eight different host species was tested by transplanting detached dodder stems with growing tips onto each of 30 Malosma laurina (Anacardiaceae), Anemisia califarnica (Asteraceae), Brassica cf. nigra (Brassicaceae), Rhamnus crocea (Rhamnaceae), Lotus scoparius (Fabaceae), Sambucus mexicanus (Caprifoliaceae), Platanus racemosa (platanus), and Eriogollum fasciculatum (Polygonaceae). Coiling response, or investment in a host species, was observed every 2 hours for the first 2 days after transplant, and 70 once a day, in the evening, on the 3rd and 4th days. Initial length in coil, the measure of coiling response, was determined as the length of parasite stem in coil at the end of the 4th day. This experiment is outlined in Chapter 1. Host abundance I derived host abundance for the 8 target species from a modified Braun-Blanquet score of cover-abundance of all species in thirty-seven 4 m x 30 m transects (see Table 3 for the categories of the index). The transects were laid in 3 lines from the top of the east side of the canyon to the west edge of the canyon bottom, and traversed the areas in which C subinclusa is most common. A number between 180 and 360 was chosen from a random number table as the direction in degrees of the initial transect in each transect line. At the end of ~be 30 m transect, 2 random numbers were chosen for direction (from 180 to 360) and number of paces (from 1 to 100) to the next transect. This process was repeated until blocked by the sheer western wall of Bell Creek Canyon. The second transect line began 100 m south of the first line and the 3rd line 100 m south of the 2nd, with 14, 13, and 10 transects, respectively. Relative abundance was calculated as mean rank over all 37 transects. At the same time I scored a transect, I also recorded the number of infested and uninfested M. laurina individuals within the transect. 71 X-section Overview c. of habitat of habitat $ubineluu :!'Uflna Q ~\. ~·~ubinelusa ••••. ~ _~U~~~~~~'- .... 0 . M.i Jan-Mar laurina Q. r-~~,.~ ~t-.4 .. ~- Apr-May Q '*t-aJun-Jul ~k.. __ Aug-Oct Q~. • "'-T.. ,*1~~ ". 0 .• - Nov-Dec Figure 14. C. subinclusa growth and phenology during a year. A parasite initially establishes on M. /aurina during winter or early spring. It accumulates biomass as the weather warms, infesting additional basts, until the onset of flowering in late August. Prior to flowering, dodder dies back to tissue closely appressed to the host branches, where the flowers and fruit are formed. During the late fall and winter scattered remnants of living parasite tissue survive on M. laurina bushes. 72 Proximi1;y to Malosma I calculated the average proximity to M. laurina of each of the 8 target host species by analyzing ground cover between 102 pairs of M. laurina. The particular pairs measured were chosen from an ongoing demographic study of dodder individuals infesting M. laurina. I measured the ground cover between the infested M. /aurina and the nearest infested and uninfested M. laurina individuals, then the cover between the uninfested M. laurina of this trio and its nearest uninfested neighbor. These measures represent the route a dodder individual was most likely to have followed as it grew from one over-wintering host to another. From these data I determined the distance between the edge of a M. laurina canopy and the leading edge of the canopy of the nearest individual of the host species in question. Proximity to M. laurina was set equal to the reciprocal of the mean of the above distance so that a potential host species which is, on average, closer to a M. launna bas a greater proximity value than a more distant species. Three of the 8 host species for which coiling response was known did not occur along the transects used to measure cover and for these species proximity was set equal to O. RFSULTS Initial coiling response of dodder does not predict the observed patterns of host use in the field. There was no correlation between coiling response of an individual stem to a host and average host use (r = 0.3984; p = 0.3283; N = 8; Figure 15). Relative reward from a host also did not predict the extent to which 73 _ 4 1 U) OJ ~ p= 0.3283 (3 OJ I.e r= 0.3984 g; 3 I··- ti 1 !f a: OJ a. 2 OJ U) :> z OJ ""::; 1.5 2.5 INITIAL LENGTH IN COIL (em) Figure 15. Correlation between individual response of C. subinclusa to a host species and the population level patterns of use of that species. Sample sizes used to calculate means were 67 parasites for host use and 30 stemslhost species for coiling response. Bars represent ± 1 S. E. MA = Malosma laurina; LO = Lotus scoparius; AR = Anemisia califonzica; RH = Rhamnus crocea; ER = Eriogonum Jasciculatum; BR = Brassica cf. nigra; PL = Platanus racemosa; SA = Sambucus mexicana. 74 Table 3. Categories of host cover index. The index has been adapted from the Braun-Blanquet index of plant cover (in Mueller-Dombois and Ellenberg 1974). not occurring in transect 0.2 solitary, with small cover 0.7 few, with small cover numerous or scattered with cover .5.. 5% 5-25% cover 25-50% cover 4 50-75% cover 75-100% cover 75 host species were infested. Biomass accumulation of C. subinclusa was greatest when growing on M. laurina. Nonetheless, only 11 of the 229 M laurina individuals occurring within transects were infested by the parasite, while all 5 species on which C subinclusa accumulated less biomass during the growing season were also used. In addition, dodder grew more when infesting Platanus racemosa and Sambucus mexicana than Eriogonum fasciculatum, yet the parasite was found growing on E. fusciculatum during this survey and not on either of the other two species. Untransfonned means, standard errors. and sample sizes of host use and host abundance, as well as distance from and proximity to M. laurina, are presented in Table 4. In contrast, descriptors of the vegetation explain much of the variation in host use by C. subillclusa. The more common a species was, the more likely it was to be infested by the parasite; abundance in the habitat explained 78% of the variation in host use by the parasite (r = 0.8804; P = 0.0079; N = 8; Figure 16). Proximity of a host species to M. laurina was also a Significant predictor of host use by the parasite: host species that were on average closer to M. laun'na were more likely to be infested (r = 0.95117; P = 0.0010; N = 7; Figure 17). However, mare abundant species were also, on average, closer to M. laurina (r = 0.8826; P = 0.0085; N = 7; Figure 18), and several tests were necessary to ascertain the independent effects of host af}undance and average distance from a M. laun'na individual. Two partial correlation models revealed that when the effect of abundance of a species was controlled far, species more proximate to M. laun'na were still significantly more likely to be infested than 76 Table 4. Mean values of host use, host abundance in the habitat, distance from and proximity to the sustaining host, and patch size. Figures represent X (N) ± S.E. For host use and abundance, sample sizes are the same among species. Distance Proximity from to Patch Host Use Abundance Malosma Malosma Size N=67 N=37 (m2) em lid em Malosma 3.849 1.622 113.73 (11) laurina ± 0.371 ± 0.15 ± 10.66 Lotus 3.104 1.486 22.85 (72) .0438 95 (113) scoparius ± 0.464 ±0.19 ±6.6 ±8.3 Rhamnus .221 .461 122.31 (13) .0082 61 (4) crocea ± 0.040 ± 0.11 ± 14.16 ±5.8 Artemisia .9254 .830 103.13 (40) .0097 58 (61) califomica ± 0.436 ±0.07 ± 12.40 ±6.4 Eriogonum .0085 .592 149.25 (8) .0067 34 (10) [asciculatum ± 0.008 ±0.08 ± 12.04 ± 5.1 Brassica .0038 .146 -0- c[. nigra ± 0.003 ±0.04 Platanus .0000 .135 -0- tree racemosa ± 0.08 Sambucus .0000 .027 -0- tree mexicana ± 0.02 77 .8 + W r = 0.8860 ~ .4 P =0.0024 '"g .2 O+*~~~-r------~{~"------~------~------~ o .1 .2 .4 .5 LOG(ABUNDANCE + 1) Figure 16. Correlation of host abundance in the habitat and average use by C. subinclusa. Sample sizes used to calculate point values, untransformed means, and standard errors are presented in Table 4. See Figure 15 for key to species names. l 78 .8 .6' ~ + w r=O.9512 (J) ::l .4 P =0.0073 0 "-' .2 o S~ ____EL:_~ _____~ ____~ ____~ o .005 .01 .Q15 .02 LOG(PROXIMITY t 1) Figure 17. Correlation of average host use and proximity of that species to M. laurina. Sample sizes used to calculate each point value, untransformed means, and standard errors, are presented in Table 4. Because proximity is the reciprocal of distance, there are no standard ereror figures for these values. See Figure 15 for key to species names. 79 ;: 015 r", 0.8826 > p= 0.0085 !:: ::; oX .01 a: fl. G g ,005 .3 .4 LOG (ABUNDANCE + 1) Figure 18. Correlation between species abundance and proximity of that species to M laurina. Sample sizes used to calculate point values, untransformed means, and standard errors are presented in Table 4. See Figure 15 for key to species names. 80 species more distant from this host (r = 0.7761; P = 0.035; df = 4). On the other hand, when the effects of proximity of a host species to M laurina was held constant, there was no longer a significant relationship between species abundance and its use by C. subinclusa as a host (r = 0.3207; P = 0.268; df = 4). Additionally, host abundance, when aqded to host proximity in a regression model host use, did not significantly increase the explanatory power of the model (from 90% to 91%; P > 0.75). However, in the reciprocal analysis, adding host proximity to a regression of host abundance and host use did increase the variation in host use explained (from 78% to 91%; P = 0.076). To test the linearity of the relationship between host use and host abundance, an orthogonal polynomial was created by adding the term (lag(abundance + 1) - mean lag(abundance + 1))2, the square of the residual of abundance, to the original linear equation explaining host use (Sakal and Rolf 1980). Comparison shows that the higher order equation does not explain significantly more of the variation in host use (2 = 0.79 for th~ linear correlation, p = 0.0079 versus 2 = 0.41, P = 0.0893 for the polynomial equation), and I conclude that the relationship between host use by C. subinclusa and host abundance in the habitat is not significantly curvilinear. Once the effect on host use of proximity of a host species to M. launna was assessed, preference of C. subinclusa accounted for an additional 7% of the remaining variation in host use (from 90% to 97%; p < 0.02). In total, 97% of the variation in average host use was accounted for by average distance of a host from M. launlla and the coiling response of the parasite to a 81 host (r = 0.9862; P = 0.0007; N = 7). DISCUSSION The largest single determinant of host use by Cuscuta subinclusa is the average proximity of a potential host species to Malosma laurina, the primary host. The closer a species is, on average, to a M. laurina bush, the more likely it is that C subinclusa will be found growing on it (Figure 17). Of the remaining variation in host use, a significant amount is explained by individual coiling response of the parasite to a host species. It is important to note here that when tested alone, individual response does not predict host use (Figure 15). Individual investment is a relevant factor in host use only after distribution of hosts in the habitat is accounted for, suggesting that the mechanisms possessed by dodder to better exploit hosts are effective only after contact is made with a host. This study of resource use in C subindusa has been guided both by predictions based on foraging theory and on information derived from studies of herbivorous insects. Although foraging theory can be used to describe the response of the individual dodder stem to a host, this is not adequate to predict population level patterns of host use. Foraging theorists generally assume random encounter of forager and resource (Pyke et al. 1977; Krebs 1978; Krebs et al. 1983; Pyke 1984; Stephens and Krebs 1986; but see McNan: 1979; Mitchell 1986). This is not always an unreasonable assumption if both predator and prey are mobile organisms. However, for herbivores, resources are neither mobile nor likely to be randomly distnbuted (Greig-Smith 1983). Even with • forager as 82 vagile as a bird, resource distnbution can change the perceived value of the reSQurce (Moermond and Denslow 1984). How much more important resource distnbution must be in "foraging' plants (and invertebrates) which are even morc likely to suffer sensory limitations and mObility constraints relative to the distribution of the resource. Internal constraints have been incorporated into foraging mcc:tels as search or handling costs, and have successfully descnbed the individual behavior of a foraging organism (Krebs 1978). Nonetheless, as this study points out, individual traits and constraints may not be sufficient to predict population level patterns of resource use. Detailed information of the specific habitat of C. subinclu.ra was necessary in order to explain host use in the observed population of parasites. In contrast to studies of foraging, studies of insect herbivory have focused on population level patterns, both because of the economics of pest control, and because of the difficulty of tracking a small, rapidly moving object over large distances. Although great strides are being made in understanding the mechanisms of specific behaviors (eg. Bach 1981, 1984; A1unad 1983; Denno and McGure 1983), the study of these behaviors in the field remains extremely difficult. The extent to which C subinclusa is analogous to an insect herbivore suggests to me that knowledge of dodder may be applied profitably to studies of berbivory in insects. An individual C. subinclusa offers a unique advantage in that it leaves an unequivocal "trail'l of its decisions. A coil once made, is never unmade and stems connect the sequence of hosts exploited in the past. Even when a host dies, or a coil is no longer functional, the dried parasite tissue is still 83 visible to the naked eye; coils without external parasite tissue still have a row of black spots corresponding to entry sites of haustoria. Because I was able to follow the "trailll of C. subinclusa individuals, I have been able to sbow conclusively that host use by C subindusa is best explained by the spatial array of hosts in the babitat, specifically, the average distance of a species from the sustaining host, M. laurina. Prior to this, several studies have suggested that proximity of a resource may influence the probability of its being included in the diet of a Don~monophagous herbivore; however, these data have not addressed the issue directly. Rather, the studies in question have focused on the probability of a plant being attacked by an herbivore, demonstrating that the species composition and density of the area immediately surrounding a plant can affect the chance of infestation. For example, herbivores can "overflow' from a more preferred host species to a less preferred species (Thomas 1986). Neighbors may also influence the intensity and probability of herbivory by grasshoppers (Holmes and Jepson-Innes in press). It has also beeo suggested that plant neighbors may harbor predators of herbivores, and thus influence infestation rates in this manner (Atsatt and O'Dowd 1976). My study, by explicitly asking whether or not an item is likely to be included in the "dietll of an herbivore, has shown the importance to an herbivore of the spatial array of hosts in the field. To C subinc/usa, resource abundance is important in resource use only insofar as it contnbutes to proximity of a host species to M. laurina. C subinclusa is most likely to make contact with a more abundant species because more 84 abundant species are, on average, closer to a M. Iaurina bush, the point of origin of all infestations. This suggests that generalist herbivores may use more abundant species (e.g., Singer 1983; Rowell 1985) not only because the species is more likely to be found, but because it is more likely to be found first. If this is true, then for generalist herbivores, a more dispersed host species is likely to be infested more frequently than an equally abundant and acceptable, but aggregated, species. A response such as this would have implications for the design of poly-cultures for insect pest management (e.g., Risch et al. 1983). Evidence shows that for some insect herbivores, discrimination among resources decreases with time (Singer 1982; Rauscher 1983). One result of this response could be that a closer resource is accepted, even though it is less valuable in terms of growth response, simply because it occurs within this window of lessened discrimination. This is indeed the case for gypsy moth larvae (Barbosa 1978) and winter moth larvae (Wint 1983). For a highly specialized insect this logic may not apply. It only says that the insect will exploit the first appropriate patch found. But for an oligophagous or polyphagous herbivore this leads to the conclusion found in this study, that probability of infestation for a host species may depend on proximity to the origin of the parasite. The observed patterns of host use by C. subinclusa probably reflect constraints on mobility specific to this species. With C. subinclusa, an unsupported growing tip and the stem attached to it are rarely more than 35 em long (Kelly pers obs); much beyond that length and the tip must have support in order to continue horizontal expansion into the habitat. In the Coastal sage scrub 85 where C. subinclusa occurs, the shrubby species that serve as hosts to dodder grow in patches of 0.3 m diameter or more (fable 4). Thus C subinclusa coils upon (infests) a host because it has reached the point beyond which it would be too costly to "travel" further without a host. In this particular case, that distance is apparently determined hy the need for support, but the coostraint could equally well be calories, or life-span, or any number of things. In an earlier paper, I showed that use of hosts in the Costa Rican dodder C costaricensis differed significantlY from abundance of those hosts (Kelly et aL in press). Although these results appear to contrast with the relatiooship between abundance and use of hosts by C. subinclusa descnbed in this paper, this difference may actually support the above biological explanation. In the habitat in which C costaricensis occurs, vegetative cover is continuous, with patch size of host types much smaller than in the southern California habitat of C subinclusa. Because of these two factors, I postulate that the difference in tbe effect of host abundance on the two species is because C costaricensis can "overreachll a host patch before the parasite must coil for support. The shorter distances between patches of a particular host type may also be viewed as lowering search costs (growth costs), allowing greater discrimination between host types and rejection of less valuable hosts (see Kelly in review for discussion of search costs). Different analyses were used in the two studies and the different conclusions as to the relationships between host use and host abundance for the two species might have been due to this. For C. costaricensis, host use was compared to host abundaoce hy an ANOVA of the ratio of use to availability for 86 the 10 host types. Reanalysis using the regression method shown in this study produces a significant positive relationship between use and abundance of hosts of C costaricensis, as the case for C subinclusa. However, host abundance explains much less of the variance in host use for the Costa Rican dodder than for the Californian species (r' = 0.40; p = 0.05 versus r' = 0.78; P = 0.002, respectively). suggesting that regardless of the method of analysis used, there are real differences in the ecology of host use by the two species that result in differences in the impact of host abundance on host use. The traits of C. subinclusa that maximize exploitation of a host can come into play only after contact between host and parasite is made. As with insect herbivores, C. subinclusa possesses mechanisms to gauge and respond appropriately to a host once discovered. The extent of coiling by the parasite is proportional to the expected reward from that host species. C. subinclusa also branches more when growing on nutrient-rich hosts. Increased branching creates more growing tips, and allows greater exploitation of the area immediately surrounding a coil. This branching response can be likened to the increased turning rate of some insects when a resource has been found (e.g., Banks 1957; Dixon 1959; Chandler 1969; Pyke 1978). a behavior that allows greater exploitation of a restricted, resource-rich area. The regression model presented here thus reflects the particular biology of C. subinclusa in that individual response to a resource is only effective (statistically significant) after habitat effects are accounted for. 87 In summary, I have shown that proximity of a resource is the primary determinant of resource use by this non-monophagous herbivore. Further, resource abundance is important in resource use only insofar as it contributes to the proximity of a resource to the point of origin of the parasite. 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