inflorescence spiders: a cost/benefit analysis for the host

Oecologia (Berl) (1982) 55:185-191 Oecologia �9 Springer-Verlag 1982

Inflorescence Spiders: A Cost/Benefit Analysis for the Host Plant, Haplopappus venetus Blake (Asteraceae) Svata M. Louda* Biology Department, San Diego State University, San Diego, CA 92182, USA

Summary. Predators on flower visitors, such as spiders, could influence plant reproduction by determining the balance between pollination and seed predation by insects. This study examines the net effect of predation by the inflorescence spider, Peucet& viridans (Hentz), for seed production by a native plant species on which it hunts. Both pollination and seed set of Haplopappus venetus (Astera- ceae) were reduced on branches with spiders; however, the release of viable, undamaged seed was higher on inflorescence branches with spiders than on those without. Occur- rence of P. viridans was associated with the flat-topped inflorescence branch structure characteristic of H. venetus rather than with the vertical structure of its congener, H. squarrosus. Thus, the interaction should be a reinforcing selective pressure on inflorescence branch morphology of H. venetus over time. Two factors providing constraints on the degree and rate of coevolution of the plant-spider interaction are suggested by the results: (1) the critical role of phenological synchrony and (2) the opposing requirements of interacting species and of subsequent life history stages within a species.

Introduction

Interaction with insects can be an important aspect of plant biology (Harris 1973). Not only are many plants dependent on insect visitation for pollination (e.g. Faegri and van der Pijl 1971 : Richards 1978) but, in addition, most plants are subject to insect herbivory (Salisbury 1942; Whittaker 1979), The visual and spatial concentration of floral resources that are necessary to attract pollinating insects (Baker and Hurd 1968) also make floral and developing seed tissues conspicuous to flower- and seed-feeding insects. Consumption of floral tissue and unreleased seed can have an important effect on plant fecundity (Salisbury 1942; Janzen 1971; Bohart and Koerber 1972; Harper 1977; Louda 1978; Lamb 1980; Zimmerman 1980b) and on plant establishment (Louda 1978, 1982a, b, 1983).

Predators on flower visitors could influence the balance between the opposing processes of insect pollination and insect-caused predispersal seed predation. The role of higher order interactions in plant reproduction is not well known (Cates et al. 1977; Price et al. 1980). On the other

* Present address: Duke University, Pivers Island, Beaufort, NC 28516, USA

hand, it is known that spiders show a numerical (Green- stone 1978) or reproductive (Wise 1975, 1979) response to increased prey density in specific cases, and insects on plant inflorescences do provide temporary increases in prey concentration. Several families of spiders characteristically hunt on flowers (Comstock 1940; Marden 1963; Gertsch 1979; Morse 1979, 1980), and these predators may be "part of a plant's battery of defenses against herbivores" (Price et al. 1980). However, such predator defense against inflorescence herbivores carries an implicit cost, the potential reduction of pollination by insects; predation by spiders may be analogous to interference by ants with pollinators or with plant parasites in ant-plant mutualisms (Carroll and Janzen 1973; Bentley 1976; Messina 1981 ; Skinner and Whittaker 1981).

If the balance between pollination and predation by insects is positive for the plant when a spider is present, one would predict selective reinforcement of traits, such as morphological adaptations, which attract spiders and which reinforce the interaction and facilitate the mutualistic relationship between the plant and its defenders (Janzen 1967). Few relevant studies exist to test this hypothesis. Furthermore, data on such higher order interactions may provide insight into constraints on the degree and the rate of coevolution among interacting species.

The purpose of my study was to examine the effect of predation by the inflorescence spider, Peucetia viridans (Hentz), on seed production by a plant, Haplopappus venetus Blake (Asteraceae), on which it hunts. The central question was: what is the net effect of predation by P. viridans on inflorescence insects for the reproductive output of H. venetus? This involved two subsidiary questions: (1) is pollination decreased significantly in the presence of an inflorescence spider? and (2) is destruction of floral tissues and seeds by insect seed predators reduced significantly by spider foraging? In addition, I asked whether there was an association between spider occurrence and inflorescence branch structure. I hypothesized that: (1) localized foraging by P. viridans was consistent with optimal foraging theory and contributed significantly to observed variation in seed set and seed release by H. venetus (Louda 1978, 1983); and (2) the morphological form of the inflorescence branch of H. venetus was attractive to spiders, enhancing continued interaction and net positive outcome for the plant. Conse- quently, data were collected on spider occurrence on H. venetus, with a flat-topped inflorescence branch (Fig. 1 A), and on a closely related co-occurring species, H. squarrosus

0029-8549/82/0055/0185)$01.40

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Fig. 1. Inflorescence branch structure of Haplopappus. A=H. venetus Blake, B = H. squarrosus H.&A.

H.&A., with a vertical inflorescence branch (Fig. 1 B) and with higher pollination and predation rates in the same climatic area (Louda 1978, 1982a, b).

System Studied

I. Host Plant

Haplopappus venetus Blake is a small shrub, 50-150 cm tall, that is characteristic of the coastal sage scrub vegetation from central California to central Baja California, Mexico (Munz and Keck 1959; Mooney 1977). H. venetus occurs primarily in disturbed microhabitats, such as alluvial fans, arroyos, and overgrazed horse pastures. Vegetative growth occurs in winter and spring. In July, flower heads are initiated and flowers occur in August-September; seeds are released in October-November (Fig. 2).

2. Study Area

The main study site was a coastal, disturbed plot at the junction of Carmel Valley Road and Interstate Highway 5 in Del Mar, California, 22 km north of the City of San Diego. This site was adjacent to the back of Penasquitos Lagoon, an area with some of the largest stands of H. venetus observed in San Diego County. Site characteristics and vegetation description are presented elsewhere (Louda 1978).

3. Inflorescence Spider Peucetia (Oxyopes) viridans (Hentz), the Green Lynx Spider, is the most conspicuous and common member of the Oxyopidae, occurring in the southern United States, Mexico, and Central America (Gertsch 1979). The adults (female= 14-16 mm body length, male= 11-13 mm) are diurnal, visual hunters that forage on plants (Gertsch 1979). Western specimens of P. viridans are often associated with wild buckwheat, Eriogonum fasciculatum (Brady 1964; M.H. Greenstone, personal communication). Maturation and mating occur in August (Comstock 1940). Egg sacs are constructed in September-October (Whitcomb et al. 1966; Louda, personal observation) and are defended pers- istently by the female until spiderling emergence (Gertsch

1979). Consequently, female spider site tenacity is excep- tionally high, from bud initiation through seed release. The newly hatched first instars remain in the egg sac 12-14 days before they molt and leave the sac (Whitcomb et al. 1966). The spiderlings thus emerge at the end of September or beginning of October (Lowrie 1963; Louda, personal observation). The newly emerged spiderlings feed and eventually disperse, overwintering as second or third instar spiderlings. Seven to 9 instars (286-301 days) are required to reach ma- turity (Whitcomb et al. 1966).

4. Flower Head Insects Three groups are attracted to the flower heads: phytophagous species, parasitoid/hyperparasitoid species, and pollen or nectar foraging species. At least eleven phytophagous species forage on the developing flowers and seeds (Louda 1978, 1983). The most conspicuous are three tephritid flies: Urophora formosa Coquillet, Trupanea femoralis Thomp- son, and Paroxyna murina Doane. The most destructive phytophagous species are microlepidopterans in three families: Pterophoridae, Tortricidae, and Gelechiidae (Soph- ronia sp.). In addition, the developing ovules are fed on by larvae of two pteromalid wasps and of a curculionid weevil, Anthonomus ochreopilosus Dietz. Additionally, the flowers attract phytophagous thrips: Frankliniella occidentalis (Pergando), F. minuta (Moulton), and Thrips tabaci Lindeman. The phytophagous insects attract parasitoids and hyperparasitoids. A eurytomid (Eurytoma sp.), a eulopid (Tetrasticus sp.), and a parasitoid species of pteromalid attack the tephritid flies. An ichneumonid parasitoid attacks the moth larvae. Finally, the pollen and nectar for- agers attracted to the flower heads include honey bees (Apis mellifera), a chrysidid wasp, and a halictid bee.

Methods

Plant Phenology

Development of flower head buds, flower presentation and seed maturation were recorded for all heads on three inflorescence branches on each of three plants (N= 9 branches). The censuses included growth and number of flower heads in five developmental stages and were done biweekly from 22 July to 27 December 1976. Developmental stages of flowers and seeds were defined as follows: (1) small buds were heads less than 4.0 mm total length; (2) large buds were unopened heads from 4.0 mm up to presentation of floral buds and less than three opened flowers; (3)flowering heads were those with at least three florets with open, bright yellow floral tubes; (4) maturing heads were those with fewer than three fresh flowers but with no more than two seeds missing and released; and (5) releasing heads were those with more than two seeds dispersed but at least two seeds remaining in the head. Following the latter stage, the heads were considered empty.

Arthropod Phenology

Insect seed predator occurrence was sampled biweekly by collecting ten heads in each developmental stage (N= 50/ date). These were collected from plants intercepted along a random transect. Up to five heads, a maximum of two in any developmental stage, were taken from an individual plant. These heads were returned to the laboratory and dissected within 24 h. In addition, marked plants (N= 15)

were examined biweekly and spider occurrence was recorded. Estimates of the relative frequency of Peucetia viridans on both H. venetus and the closely related H. squarrosus were made (25-28 October 1978). Plants were measured and presence or absence of a spider was noted for all plants taller than 50 cm ( N = 150 individuals/species).

Seed Production in Relation to Spider Presence

Every H. venetus individual over 50 cm tall within a 2 m x 25 m transect was examined on 1 2 November 1977 to evaluate seed product ion and damage in relation to spider presence. The tallest central flowering branch for twenty, equal- sized plants, ten with and ten without P. viridans, were collected and dissected in the laboratory . I recorded the total number of heads, their developmental stage, and damage. All flowers ini t iated and ovules present were scored for size, stage, and condi t ion (Louda 1978). Identical proce- dures were used to evaluate seed destruction on H. squarrosus (Louda 1978, 1982a, b).

R e s u l t s

Spider Occurrence

Spiders were associated with larger individuals of H. venetus rather than with earlier plants or with larger inflorescence branches among plants. H. venetus size, measured as maximum height and as total branches per plant, was greater for those plants with adul t spider than for those without spiders (Table 1). F lower phenology was similar between the two groups, and product ion of flower heads for sampled plants was the same (Table 2). The flowering phenology was similar between branches with and without spiders (Ta- ble 2). In addit ion, the p ropor t ion of heads which had dispersed their seeds by the sampling date was not significantly greater, i.e. earlier, on those branches with spiders than for those without (Table 2). Consequently, spiders occurred on larger plants rather than on plants with larger or earlier terminal inflorescence branches.

Within an individual plant, however, the occurrence of P. viridans was related to the flowering phenology of branches. First , 47 of the 49 adul t spiders (95%) on the seed product ion transect were on the p lant ' s tallest flowering branch. Second, for plants observed in 1976 (Louda 1978), the tallest flowering branch was also the first to flower (93.3% of the time, N = 15 plants/site, 3 sites). So, spiders were associated with the inflorescence branch of a p lant that had the earliest vegetative and floral development.

F lower development and spider appearance on the tallest branch of a p lant coincided. Flower anthesis ranged from late August to the end of October (Fig. 2). The pre- dominant flowering period, when the highest p ropor t ion of heads were in the flowering stage (38%, N=941) , was between 21 September and 7 October (Fig. 2). A t the same time, the cumulative frequency of spiders observed on experimental plants reached over 50% (54%, N = 2 6 ) by 1 October and 65% by 7 October (Fig. 3). Spiders increasing- ly utilized inflorescences as flower development accelerated; relative abundance of adul t spiders was correlated with the relative frequency of the flowering stage (Fig. 3: Spearman Rank Correla t ion Coefficient = 1.0, P_-< 0.05).

The adul t spiders occurred on both species of Haplopap- pus; however, they were significantly more frequent on H. venetus, which has f la t - topped inflorescence branches (Fig. 1 A), than on H. squarrosus, with vertical inflorescence

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Table 1. Occurrence of an adult spider in relation to host plant size: 150 Haplopappus venetus plants were examined at the Carmel Valley Road site 25-28 October 1978

Parameter Without spider With spider (N= 101) (N= 49)

)? SE .g SE p a

Branches per plant 48.3 3.19 99.4 4.37 *

Tallest flowering 50.6 3.57 97.1 3.78 * branch height (cm)

a Mann-Whitney U test, * =P<0.05

T a b l e 2. Flower head production and damage in relation to the occurrence of adult Peucetia viridans on the tallest flowering branch of equal-sized individuals of Haplopappus venetus a at the Carmel Valley Road site on 1 November 1977

Number produced/Branch Branch p c

(N= 10/treatment) Without With spider spider

2 SE 2 SE

For all flower heads initiated b Total number 78.9 9.86 81.8 8.12 ns Number damaged 67.9 10.17 45.8 6.51 *

By head developmental category

Small flower heads Total number 14.8 0.94 15.8 1.70 ns Number damaged 11.3 1.20 13.1 1.63 ns

Maturing and releasing heads

Total number 53.7 8.88 53.9 5.41 ns Number damaged 51.5 8.93 27.7 4.97 **

Empty, released heads Total number 10.4 1.97 12.9 1.61 ns Number damaged 5.1 0.85 4.3 0.47 ns

a Mean size (height) of sampled plants: with spider=95.6 cm (SE=2.87) and nearest, equal-sized without spider=89.1 cm (SE=2.56)

b Partitioned in subsequent section by size and stage of development at the end of the season: (1) small heads were __<0.4 cm involucre, (2) large heads were > 0.4 with maturing and/or releasing developed seeds, and (3) empty heads were large heads that had released all of the matured seeds.

c Mann-Whitney U Test, * =P<0.05 and ** =P<0.01

Small B u d s

Large B u d s

Flowering

Maturing

Releasing

Empty

iiiinJllt I . . . n n

I

I

n l l l l l l l I n n n n l

Iiiiiiiii i IIiiiiii

: i i i lUl I I I IIIIInl I

i i i i i i i i

: III,~III

A S 0 N 1 9 7 6

I D

Fig. 2. Phenology of flower head, flower, and seed development for Haplopappus venetus at the Carmel Valley Road site (1976): range of occurrence of each stage and two week period of predomi- nance of each stage, when the highest numbers of the stage were observed. See text for stage definitions

188

1.00 -

• 0.75- |

0.50-

.2

0.25-

�9 - - Q Spiders H-roll Flowers 0-...0 insects

m - -7...~.~ ~

// Y

.... o , ' ; ~

l i I

l A S 1 9 7 6

I I I I

0 N

Fig. 3. Cumulative occurrence over the flowering season of adult Peucetia viridans individuals (e), open flowers of Haplopappus venetus (u), and immature insect seed predators (all stages) in flower heads of H. venetus (o) at the Carmel Valley Road site, 1976

. . . . . Tephritid Flies 0 - - 4 ~ Other Insects

0.7-

I i 0 .5 - I k /?-,

/ \ ."~ / / i \.

J A S 0 N

1 9 7 6

Fig. 4. Relative frequency of tephritid flies (e = eggs, larvae, prepu- pae and pupae) and other insect seed predators ( . = all stages) in flower heads of Haplopappus venetus at the Carmel Valley Road site, 1976

branches (Fig. 1B). Of the 150 H. venetus examined at the coast in late October 1978, 32.7% had at least one adult Peucetia viridans spider. Most of these (98.0%) were territo- rial, persistent females with egg sacs. Among the 49 adult P. viridans observed on H. venetus, 95% were on the tallest

flowering branch of the plant. In contrast, only three of the 150 H. squarrosus plants examined at the same time (2%) had an adult spider. Two of the three were females tending an egg sac.

Interaction with Insects

An increase in spider frequency (Fig. 3) accompanied an increased probability of flower visitation by both pollinators and seed predators. Cumulative frequencies of adult spiders and of flower- and seed-feeding insects in all stages of development were identical between mid-September and mid-October (Fig. 3). The frequency of immatures (all stages) of the seed predators was highest in this period (Fig. 4). The increase initially reflected oviposition by tephritid flies between 15 September and I October and additionally by other insects, especially between 1-15 October (Fig. 4). Also, peak flowering, and therefore pollinator ac- tivity, occurred during the period between 21 September and 7 October (Fig. 2).

When adult spiders were present, insects caused less damage to flower heads. The number of maturing heads and the proport ion of all flower heads that were damaged by insects were significantly lower on branches with an adult spider than on those without (Table 2). Spiders were observed capturing potential seed predator adults and inter- fering with oviposition (Louda, personal observation). In- terestingly, the number of small buds that were damaged was not decreased on branches with spiders (Table 2). Small buds appear on terminal inflorescence branches early in the season (Fig. 2), prior to the median of the frequency distribution of spiders on these branches (Fig. 3).

Spiders apparently interfered with insect pollinators. Lower levels of seed set were associated with the presence of adult spiders. The number of achenes, single-seeded fruit, set per flower head on branches without spiders was 5.4, 25-28% of the total florets initiated (Louda 1978). When spiders were present, the number of seeds set per head was between 3.6 and 3.9, 17- /8% of florets initiated (Table 3). In addition, spiders were observed both capturing flower visitors and interrupting visitation (Louda, personal observation). Thus, it is likely that spiders were responsible for the reduction in the proport ion of flowers which were pol-

Table 3. Flowers produced and seed set on the tallest flowering branch of Haplopappus venetus in relation to the presence of the spider, Peucetia viridans, at Carmel Valley Road on 1 November 1977

Number/Flower head Tallest flowering branch p" Without spider With spider

N 5( SE N R SE

Total flowers initiated/Head b In heads with no insect damage 110 19.1 0.87 375 19.6 0.29 ns In heads with insect damage c 679 22.0 0.69 451 21.8 0.88 ns

Total pollinated flowers/Head d In heads with no insect damage 22 5.4 0.68 262 3.6 0.49 * In heads with insect damage c 515 5.4 0.49 277 3.9 0.38 *

Undamaged matured seeds/Headd In heads with no insect damage 22 5.4 0.68 262 3.5 0.49 * In heads with insect damage c 515 2.9 0.42 277 2.8 0.94 ns

" Mann-Whitney U Test, z approximation, *=P=<0.05 b For all flower heads, independent of stage of development

Flower heads with any evidence of insect feeding or oviposition on phyllaries, flower head receptacle, internal florets, or developing ovules and seeds

a For maturing and releasing flower heads only

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linated in a head, from around 26% to about 17% (Ta- ble 3), an average reduction in branch fecundity of about one-third.

The net effect of spiders on development and release of viable seed by H. venetus, however, was positive. On branches with spiders the lower proportion of flowers pollinated per head (Table 3) was offset by a highly significant increase in number and proportion of maturing flower heads that escaped damage by insects (Table 2). Thus, average production of viable seed on flowering branches with spiders was higher than on those without: J?=286 seeds/ branch (SE= 11.77) and J?=243 seeds/branch (SE=9.96) respectively (Mann-Whitney U Test, P<0.05). The de- crease in seed set in the presence of spiders (from 395 to 328/branch; Mann-Whitney U Test, P < 0.02) was counter- acted by an increase in seed matured (from 243 to 286/branch), a net increase of 17.7% in seed production per branch (Mann-Whitney U Test, P < 0.05).

Discussion

The essential feature of the interaction between spiders and insects for the host plant is the net outcome. The relative intensities of the spiders' interactions with flower visitors versus with insect consumers determines the influence of each group on successful seed release by the host plant. Pollination success was lower on branches with spiders, but insect damage to seeds was also reduced on those branches. The net result was an increase in the number of viable seeds matured and released where spiders were present. The impact of spiders on overall fecundity of individuals of Hap- lopappus venetus will be determined by: plant size (branches/plant), number of spiders per plant, and number of branches utilized by each spider. However, since seedling recruitment by H. venetus was directly proportional to the number of undamaged seeds released under all environmental conditions examined (Louda 1978, 1983), predation by Peucetia viridans has potentially significant implications for H. venetus' reproductive success. A consistent increase in plant fecundity as the result of the higher order interaction - among spiders, pollinators, and plant predators - could lead to significant cumulative, long-term effects for the population dynamics of this native plant. The data further suggest that there is a temporal" window" for flower predators, one of the spiders' prey groups, that allows persistence and significant plant impact by predispersal predators even in the face of high densities of spiders.

Peucetia viridans is not alone in its potential for this type of indirect effect on its plant host. Parallel examples may include salticid and thomicid spider predation on the tephritid, Orellia occidentalis, developing in the flower heads of the Platte thistle, Circium canescens (Lamp 1980), and also other interactions of the Asteraceae with flower- and seed-feeding insects (Louda, unpublished data). In addition, predatory ant/plant interactions on inflorescences should have a similar cost associated with their anti-herbivore benefit. Predatory ants, responding to extra floral or floral nectar production (Carroll and Janzen 1973; Bentley 1976, 1977; Tilman 1978 ; Inouye and Taylor 1979; Skinner and Whittaker 1981) or to other plant resources such as hollow thorns for nesting (Janzen 1966, 1967), can interfere with pollinators as well as with insect enemies. These studies lead to the suggestion that the phenology of the community of plants and animals, i.e., the timing of the occurrence

of each group in the interaction, is critical to the net outcome for the plant.

The outcome of this specific set of interactions was positive for the host plant in this case, but secondary interactions need not be so. Even in this case at least two constraints were evident. First, the net outcome for the plant depends on the timing of occurrence of the spiders in relation to the timing of flowering. Even a slight variation in the phenology of the interaction would lead to one of two different results. If spider colonization had been 1-2 weeks earlier or flower presentation or development had been delayed, pollination would have been prevented. If, instead, spider colonization of the inflorescence branch had been 1-2 weeks later or flower presentation had been early, seed predation would not have been reduced. The timing, which is critical to the net effect on the host plant's seed production, reflects a variety of factors to which plant, and spider, and floral insects must respond independently. For example, since flowering phenology is influenced by both environmental and genetic factors (Sorenson 1941 ; Jackson 1966; Louda, personal observation), exact flowering time will shift between years. Independent response to environmental conditions has the potential of changing the relation of flower presentation and spider occurrence and, thus, provides a potential constraint on the development of the interaction. Second, the linkage is additionally constrained by the negative effect that complete insect exclusion from the flower heads would have on spider reproduction through lowering the potential food supply for the spiderlings. The key point, however, is that the results suggest that there are significant potential constraints on the degree of interde- pendence between the plant and the spiders.

The occurrence and timing of the adult spiders, sit-and- wait predators, were consistent with foraging and consumer theory (Roughgarden 1976; Pyke et al. 1977). An inflorescence that attracts large numbers of insects provides a localized patch of increased prey density. For a female P. viridans, location on the inflorescence branch should maximize the probability of encountering prey, particularly within the constraints of constructing and defending an egg sac. The appearance of female spiders on inflorescence branches from the foliage was correlated with increased insect occurrence there, suggesting a response by female spiders to increased resource availability. Generally, spiders' habitat preferences are influenced as much by prey availability as by physical conditions (Hallander 1967, 1970; Turnbull 1965, 1972; Riechert and Tracy 1975; Morse 1979; Olive 1980). Response to prey density is logical since food-limited reproductive success occurs and has been demonstrated for: orb spiders (Wise 1975, 1979), a lycosid (Kessler 1971), and for the agelenids Agelenopsis potteri and A. aperta (Rie- chert and Tracy 1975). My results, thus, are consistent with predicted behavior of female spiders in relation to variation in prey concentrations.

The observations of female occurrence and foraging also support the hypothesis of differential feeding strategies between male and female spiders (Haynes and Sisojevic 1966; Givens 1978), with female spiders responding primarily to prey availability. Effective female foraging is constrained by reproductive requirements, such as the site tenacity necessary in the defense of the egg sac and the establishment of the sac in a location which increases the probability of food for the young (Givens 1978). The position of female spiders, thus, must be a compromise between exposure to

190

predators such as wasps (Muma and Jeffers 1945; Kurc- zewski and Kurczewski 1968; Doris 1970; Olive 1980), predictability of prey, and reproductive needs.

Location on an inflorescence branch should have an added advantage. Food for the spider's young is high on the inflorescence branch when they emerge in October, since immature flower- and seed-feeding insects developing in the inflorescences emerge in October-November. Besides being abundant, the emerging microlepidopteran and tephritid seed predators are about the same size as the spiderlings and are especially vulnerable from eclosion to wing harden- ing. Thus, foraging and ovipositing insects provide a con- centrated resource for the adult female spider, while emerging insects provide a resource for the young spiderlings. Further work is warranted to test whether prey availability in the form of emerging, newly eclosed insects increases the sur- vivorship and recruitment of spiderlings as predicted here.

Spider occurrence was associated with a specific inflorescence branch morphology between the two related species of Haplopappus examined. The efficiency of exploi- tation may be related to the area over which the search must be conducted. Haplopappus venetus, the plant used more frequently, has a flat-topped, horizontal flowering branch (Fig. 1 A); those of Haplopappus squarrosus, an in- frequently used but available plant, are predominantly of vertical orientation (Fig. 1 B). While variation in inflorescence branch form occurs within both species, the interspe- cific difference is distinct and characteristic (Fig. 1A, B). It is interesting to note that Eriogonum fasciculatum, another southern California plant on which Peucetia viridans hunts (Brady 1964; M.H. Greenstone, personal communication), also has a distinctly flat-topped inflorescence branch which is similar in form to that of H. venetus (Fig. 1A). The horizontal form increases the spatial concentration of flowers and, thus, the probability of encountering flower visitors. The spatial concentration of insects is greater on a flat, horizontal inflorescence branch since the surface area of that configuration was less than that of a cylinder composed of the same number of flower heads in a vertical arrangement. Thus, plant morphology influ- ences prey availability and provides a characteristic to which the spider can respond.

The main alternative hypothesis to explain greater spider occurrence on H. venetus is that insect visitation and prey abundance are higher on H. venetus than on H. squarrosus. This hypothesis appears unlikely for two reasons. First, the level of seed predation in coastal areas is higher on H. squarrosus than on H. venetus (Louda 1978, 1982a, b); this suggests that both the number and the predictability of flower head consumers and their parasitoids is higher on the less frequently used form, the vertical inflorescence branch of H. squarrosus. Second, flower heads are larger and successful seed set is higher on H. squarrosus than on H. venetus in the coastal zone (Louda 1978, 1982a, b). Since there is usually a strong relationship between seed set and pollinator visitation rates (Waser 1978; Pleasants 1980; Zimmerman 1980a; N.M. Waser and M.V. Price, personal communication), higher rates of seed set on Haplopappus squarrosus than on H. venetus (Louda 1978) suggest higher insect pollinator visitation on H. squarrosus. Consequently, spider use of Haplopappus venetus over H. squarrosus must reflect something other than absolute abundance of insects on the two species. Spider occurrence, interestingly, was only very localized and differed among H. venetus plants

as well as between host plant species. This suggests that there are other factors impinging and limiting the degree to which sit-and-wait predators can exploit even relatively pre- dictable, high concentrations of insect prey on inflorescences.

Second order interactions have been postulated as a step toward coevolution and mutualism (Janzen 1967; McKaye 1977, 1979; Buss and Jackson 1979; Price et al. 1980). The usual assumption is that once an interaction is established, it is just a matter of time before the system becomes "fine- tuned". Some systems are more closely coevolved than others (Janzen 1980); we need further analysis to know why some interactions become very closely linked and others do not. In this case some constraints on tight linkage appear clear: (1) the pivotal role of phenological synchrony in the net outcome for the host plant; and (2) the conflicting requirements of plant versus spider and of adult spider versus spiderling. The work on this higher order interaction, thus, suggests two conditions which constrain the degree or the rate of coevolution of primary interactions. The short-term interaction of predator/insect/plant described here led to differences in seed set and seed loss. Spider occurrence was patchy. Such patchiness contributed additional variation in seed production. Other data on the con- tribution of higher order interactions to variance in seed set and loss among plants or frequency of their occurrence are rare. However, the findings of this study suggest that an understanding of such interactions is crucial to our ability to explain variation in successful reproduction among plants.

Acknowledgements. I thank M.H. Greenstone and P.R. Atsatt for the encouragement provided by their interest in my initial observations. I appreciate the help contributed by my doctoral committee, friends, and family to my work on Haplopappus, especially the many hours cheerfully spent on data collection by G.A. Baker and G.B. Harvey. Several entomologists generously identified the insects : G. Marsh (Curculionidae), J.A. Powell (Microlepidoptera), J. Hall (Hemiptera, Diptera), W.H. Evert (Thysanoptera), and G. Gordh (Hymenoptera). Discussions with L.P. Buss and K.R. McKaye were highly instrumental in the development of my think- ing about higher order interactions. Additional suggestions by M.H. Greenstone. J.L. Hayes, N. Huntly, D.W. Inouye, D.H. Morse, M.V. Price, M. Stanton, N.M. Waser, and an anonymous reviewer helped improve the manuscript. Support was generously provided by the Joint Doctoral Program in Ecology of San Diego State University and the University of California, Riverside, and by an N.S.F. Doctoral Dissertation Improvement Grant.

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Received April 21, 1982

inflorescence spiders: a cost/benefit analysis for the host

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