J. Phycol. 35, 483±492 (1999) PHLOROTANNIN ALLOCATION AMONG TISSUES OF NORTHEASTERN PACIFIC KELPS AND ROCKWEEDS1 Kathryn L. Van Alstyne2 Department of Zoology, Oregon State University, Corvallis, Oregon 97331 James J. McCarthy III, Cynthia L. Hustead, and Laura J. Kearns Department of Biology, Kenyon College, Gambier, Ohio 43022 Optimal defense theory (ODT) predicts antiher- Abbreviations: DM, dry mass; GDBH, growth±dif- bivore defensive compounds will be allocated so ferentiation balance hypothesis; ODT, optimal de- that the most valuable or most susceptible tissues fense theory will be best defended. The growth±differentiation balance hypothesis (GDBH) predicts that defense al- location will be a result of trade-offs between growth Plants allocate materials and energy among criti- and defense. Thus, these two theories predict op- cal functions such as maintenance, growth, repro- posite allocation patterns with respect to ``valuable,'' duction, and defense (Bazazz and Grace 1997 and actively growing meristematic and reproductive tis- citations therein). It is widely assumed the total sues. ODT predicts that meristems and reproductive amount of resources available for these functions is tissues should have higher defense levels than non- limited and all of these functions have signi®cant meristematic vegetative tissues; the GDBH predicts metabolic costs associated with them. Consequently, the defense levels of meristems and reproductive over evolutionary time there should be selection for tissues will be lower than vegetative tissues. We ex- individuals to distribute resources among functions amined allocation patterns of phlorotannins in 21 in ways that maximize overall ®tness, assuming that species of kelps (Order Laminariales) and rock- allocation strategies are not limited by physiological weeds (Order Fucales) from nine sites on the west or other constraints. coast of the United States to determine if allocation Two hypotheses have been proposed to predict patterns better matched the predictions of ODT or resource allocation to defense in plants: optimal de- the GDBH and to look for differences in allocation fense theory (ODT) and the growth±differentiation patterns among sites. Within-species differences in balance hypothesis (GDBH). ODT predicts that de- phlorotannin levels occurred in 10 of the 21 species fenses will be preferentially allocated to tissues with examined. Meristems of both kelps and rockweeds the highest ®tness value or tissues most at risk for had higher phlorotannin levels than nonmeristemat- attack (Rhoades 1979). According to the predictions ic vegetative tissues, consistent with ODT. Phloro- of this model, meristematic and reproductive tis- tannin levels in reproductive tissues of kelps were sues, which have a high ®tness value, should be bet- higher than vegetative tissues, but levels in repro- ter defended than nonmeristematic vegetative tis- ductive tissues of rockweeds were lower than vege- sues. The GDBH predicts trade-offs between growth tative tissues, indicating that allocation strategies and defense production (Herms and Matson 1992, may follow taxonomic lines. Allocation patterns dif- Tuomi 1992). According to the predictions of the fered among sites in four of the 16 species collected GDBH, actively growing tissues, such as meristems from more than one site. Differences in allocation or reproductive tissues, should produce lower quan- patterns among sites were usually changes in the ra- tities of defenses than nonreproductive vegetative tios of phlorotannins in well-defended compared to tissues. poorly defended tissues, rather than changes in Resource allocation patterns may also be affected which tissues were well defended or poorly defend- by environmental variability. Fluctuations in envi- ed. We concluded that environmental variability can ronmental conditions can produce changes in re- have large effects on the concentration of phloro- source pools within plants or affect foraging rates of tannins in algae but has limited effects on allocation herbivores (Boggs 1997). Many plants exhibit phe- patterns among tissues. notypic plasticity in resource allocation to defense, such as the production of herbivore-induced de- Key index words: allocation; chemical defenses; Fu- fenses (Karban and Baldwin 1997). Most work on cales; geographic variation; Laminariales; Phaeophy- resource allocation shifts in response to changing ceae; phlorotannins; spatial variation environmental conditions has focused on shifts be- tween major functions such as growth, reproduc- tion, and defense; little is known about shifts among 1 Received 14 September 1998. Accepted 22 January 1999. 2 Present address and author for reprint requests: Shannon tissues within those functions. Point Marine Center, 1900 Shannon Point Road, Anacortes, Tissue differentiation in seaweeds is generally less Washington 98221; e-mail [email protected]. complex than in vascular plants, making seaweeds 483 484 KATHRYN L. VAN ALSTYNE ET AL. an ideal system for testing the predictions of the gustifolia Bory (Tugwell and Branch 1989) and mer- ODT and GDBH models (Cronin and Hay 1996). istematic tissues or young tissues of the brown alga Among the seaweeds, the brown algae are particu- Zonaria angustata (Kutzing) Papenfuss (Poore 1994), larly useful in this regard. In the kelps (Order Lam- the kelps E. maxima, and M. angustifolia (Tugwell inariales) and rockweeds (Order Fucales), meri- and Branch 1989) have higher concentrations of stems and reproductive tissues are often distinctly phlorotannins than nonreproductive vegetative tis- localized; however, they can occur in different areas sues, consistent with ODT. of the thallus in the two orders (Bold and Wynne The goal of this study was to test the predictions 1985). Kelps have an intercalary meristem located of ODT and the GDBH by examining allocation pat- at the base of the blade. The meristem in rockweeds terns of phlorotannins in a large number of brown is located in the apical portion of the thallus. Many algal species across sites where environmental con- kelps produce reproductive sporophylls off the stipe ditions are likely to vary. We collected 21 species of or reproductive tissues within the blades. In rock- kelps and rockweeds from nine sites along the west weeds, reproduction occurs in apical receptacles. coast of the United States and measured phlorotan- Another feature of temperate marine kelps and nin concentrations in meristems, reproductive tis- rockweeds that makes them ideal for testing the pre- sues, and nonmeristematic vegetative tissues. The dictions of the ODT and GDBH models is they all speci®c questions addressed in this study were: (1) produce phlorotannins or polyphenolic com- Do patterns of phlorotannin concentrations among pounds. Phlorotannins are compounds that bind tissues follow the predictions of either the ODT or proteins and are ultimately derived from phloroglu- the GDBH? (2) Do allocation patterns of phlorotan- cinol (Ragan and Glombitza 1986, Steinberg 1992). nins across tissues vary among populations (sites)? They have antifeeding activity toward many, though (3) Do allocation patterns follow taxonomic lines; not all (Steinberg and van Altena 1992, Boettcher for example, are they different in the kelps and and Targett 1993), herbivores (Steinberg 1988, rockweeds? Steinberg and van Altena 1992, Winter and Estes 1992, Steinberg et al. 1995, Targett and Arnold MATERIALS AND METHODS 1998). Phlorotannins also have been hypothesized Collection sites. Kelps and rockweeds were collected over a 2- to serve a number of other functions, including pro- week period from nine sites, ranging from southern California to northern Washington, U.S.A. These sites included (1) the inter- tection from pathogens and UV damage (Pavia et tidal zone and a shallow Macrocystis pyrifera (Linnaeus) C. Agardh al. 1997). Concentrations of phlorotannins in ma- bed at depths from 2 to 10 m at Catalina Island, California (338239 rine brown algae range from undetectable to nearly N, 1188219 W); (2) an intertidal cobble beach at San Simeon, 20% of an alga's dry mass (Ragan and Glombitza California (358399 N, 1218139 W); (3) a kelp bed at 3±5 m depth 1986). Phlorotannin concentrations differ greatly off Lover's Point (368389 N, 1218569 W) near Paci®c Grove, Cali- fornia; (4) a wave-exposed intertidal promontory at Pigeon Point among species and among spatial scales, including (378129 N, 1228249 W) ;10 km north of Davenport, California; among tissue types in an individual (Geiselman (5) an exposed rocky shore at Mouda Point (418089 N, 1248109 1980, Steinberg 1984, 1985, 1989, Johnson and W) ;25 km north of Eureka, California; (6) an exposed rocky Mann 1986, Tugwell and Branch 1989, Tuomi et al. shore at Boiler Bay (448509 N, 1248049 W) ;5 km north of Depoe 1989, Van Alstyne 1989, P®ster 1992, Poore 1994), Bay, Oregon; (7) the intertidal zone of Tatoosh Island, Washing- ton (488239 N, 1248449 W); (8) a kelp bed at 5±8 m depth near among sites at scales ranging from tens of meters to the site of the former Cantilever Pier and off the ¯oating dock hundreds of kilometers (Steinberg 1989, Pavia and of the Friday Harbor Laboratories (488329 N, 1238029 W) on San Aberg 1996, Van Alstyne et al. 1998), and between Juan Island; and (9) a moderately wave-exposed intertidal site at global regions (Steinberg 1986, 1992, Van Alstyne Cattle Point (488279 N, 1228589 W) at the southern tip of San and Paul 1990, Steinberg and van Altena 1992, Tar- Juan Island. A map of these sites and a more detailed