SEASONAL CHANGES IN ZOOID SIZE AND FEEDING ACTIVITY IN EPIFAUNAL COLONIES OF ELECTRA PILOSA

Transcription

1 IN: Bryooa: Past and Present. Proceedings of the 7 th International Conference on Bryooa. JRP Ross, Editor. Western Washington University Press, Bellingham, Washington, pp Jl SEASONAL CHANGES IN ZOOID SIZE AND FEEDING ACTIVITY IN EPIFAUNAL COLONIES OF ELECTRA PILOSA Beth Okamura Smithsonian Marine Station at Link Port 5612 Old Dixie Hy., Fort Pierce, FL 3345, U.S.A. ABSTRACT Data collected during a larger study of the feeding of Electra pilosa colonies groing epifaunally on Fucus serratus revealed seasonal patterns in ooid sie and feeding activity. Mean ooid sies ere found to decrease through the summer months, hile feeding activity generally increased during the same period. These results are related to predictions based on hypotheses regarding body sie vs. temperature and on food availability. Spatially and/or temporally induced changes in ooid sie are rarely considered, despite broad implications for evolutionary and taxonomic studies. INTRODUCTION Variation in the architecture of clonal organisms has been suggested to relate to their competitive abilities and life history strategies. Jackson (1979) and Lovett-Doust (1981) proposed that the overall sies and shapes of benthic marine invertebrates and plants ere related to strategies of substratum procurement and maintenance. Variation in clones and colonies can occur at the module level as ell. Functional variation of modules has alloed for a marked division of labor in a number of organisms (e.g. scyphomedusae, hydromedusae, bryooans, anemones, ascidians, insect colonies). Recently, variation in the sie of modules that form clones and colonies has been considered. Over evolutionary time scales, the risk of mortality and the degree of clonal integration have been suggested to explain observed differences in module sie in bryooans, anemones, ascidians, and corals (Coates & Jackson 1985). Over ecological time scales, changes in prey sie and/or abundance have been considered to invoke module sie changes in suspension-feeding organisms (Sebens 1979). The sie of bryooan ooids is an important taxonomic character and i~ often used as a morphological character to indicate evolutionary change, yet spatial and/or temporal measures of ooid sie changes are rarely considered (but see Taylor & Furness 1978). Ryland (1963) provided incidental data of a latitudinal gradient in ooid sie for the genus Haplopoma. Silen and Harmelin (1976) found a similar latitudinal gradient in sie for the species ~ sciaphilum. Morris (198) noted tha~ fossil Hippothoa colonies had larger ooids in northern regions. In this paper I present observations of seasonal changes in ooid sie and feeding activity that occurred in epifaunal colonies of.electra pilosa.

2 198 BETH OKAMURA MATERIALS AND METHODS The epifaunal assemblage of the fucoid alga, Fucus serratus, has been the focus of numerous ecological investigations in Great Britain (for revie see Seed & O'Connor 1981). In the Menai Straits, North Wales, Electra pilosa is one of the three most common bryooans occurring on ~ serratus blades (Wood & Seed 198). ~ pilosa is present on ~ serratus year-round and is often overgron by other epifauna (Wood & Seed 198). In general, groth rates of bryooans are lo in inter (Nair 1962; Ryland 197; Stebbing 1971; Seed et al. 1981), presumably due to colder temperatures (Menon 1972). Recruitment of ~ pilosa to blades of F. serratus occurs throughout the year ith a possible peak in early summer (Seed & O'Connor 1981; Okamura, pers. obs.). In the early spring through summer of 1985 I collected relatively small colonies of Elec tra pilosa «2 cm 2, mos t < 1 cm 2 ) in the mid- to lo intertidal of the Menai Straits, North Wales. Colonies ere brought to the laboratory here I mapped them by draing their outline onto a sheet of acetate. I then performed a series of feeding experiments designed to assess the effects of neighboring epifaunal bryooans on feeding success. Colonies ere placed in a recirculating flo tank containing a suspension of latex particles (13 microns in diameter) and ere alloed to feed for 27 min. At the end of experiments colonies ere placed, frontal surfaces upard, in dilute sodium hypochlorite. This treatment dissolves organic contents of colonies but leaves intact the exoskeleton, membranous material, and latex particles. Latex particles remained entrapped ithin the ooids that had ingested them because of the surrounding undissolved portions of the ooid and because of their relatively high density in dilute sodium hypochlorite. The number of particles captured per ooid ere then quantified using a dissecting microscope. Very infrequently particles ere lost from oo ids during the release of air bubbles that ripped the frontal membrane as materials dissolved. Hoever, the effect of particle loss as deemed minimal because it as rare and not biased across experimental treatments. In addition to the number of particles captured per feeding ooid, the total number of oo ids per colony as determined. Nely-forming ooids at the edges of colonies ere excluded in these counts. Digitiing the mapped colonies provided measures of colony areas. To estimate the mean sie of ooids in each colony I divided the colony area values by the total number of ooids in each colony. In the analysis of mean ooid sies I excluded colonies that ere being overgron by other bryooans as this phenomenon may possibly affect ooid sie (Gordon 1972). The mean percentage of the ooids per colony that ingested latex particles and the mean number of particles captured per feeding ooid per colony ere used as measures of feeding activity. This technique may overestimate feeding activity as the method did not identify ooids that attempted to feed but ere unsuccessful. Feeding activity as determined for isolated Electra pilosa colonies as ell as colonies in association ith and being overgron by other epifaunal bryooans. As these categories ere relatively equally represented, the overall effect on feeding activity as deemed to be minimal, therefore the data ere pooled.

3 SEASONAL CHANGES IN ZOOID SIZE AND FEEDING 199 RESULTS Changes in Feeding Activity A general but nonsignificant increase in feeding activity as measured by the mean % ooids feeding per colony can be seen from early March to early July (Fig. la). Hoever, in late July feeding activity rose dramatically and significantly (ANOVA of arcsine transformed % feeding ooids vs. time: F6,22= , p <.1; folloed by Scheffe's method of a posteriori unplanned contrasts amongst means). Feeding activity, as measured by the mean number of particles captured per ooid in colonies, as significantly greater in late Mayas ell as in late July (Fig. lb) (F6,22= 35.33, p <.1; ANOVA folloed by Scheffe's method).,. ':: U a: '" a ~ U) N 2 ~ < :E 1 A! I! I I I 12.,. g 1. u a: 8. N a: U) 6. B I ~ u ;:: a: < 4. I < I 1 I () :E \ 2. ~F~M A--t""-M-t-J J---i I--F~M--+--A--+--~J---+--J--f Fig. 1. The mean % ooids feeding per colony (A) and the mean number of particles captured per ooid in colonies (B) from early March to late July 1985 (n = 8-63 colonies). Bars represent 2 standard errors about the mean. Zooidal Sie Changes Mean ooid sies in the June and July samples ere significantly smaller than in the May samples (Fig. 2) (F6 222= 4.83, P <.1; ANOVA folloed by Scheffe's method ). Zoo ids ~ampled in March, hoever, ere not significantly different in sie from those in May nor from those in the summer months.

4 2 BETH OKAMURA DISCUSSION Seasonal Patterns in Feeding Activity The to most likely environmental influences that may explain seasonal trends in feeding activity and ooid sie are temperature and food availability. Temperatures in the Menai Straits during the months of observations have been measured to range from about SoC in March up to 17 C in July (Buchan et al. 1967; O. Calvario-Martine, pers. conun.). In inter, temperatures can reach as lo as C. (During periods of aerial exposure at lo tides, bryooans ill experience a much greater range in temperature.) Peak levels of chlorophyll ere measured in April hile peak levels of phytoplankton primary productivity occurred in May (. Calvario-Martine, pers. comrn.). In general, the Menai Straits experience spring and fall blooms of phytoplankton (Jones & Spencer 197; AI-Hasan et al. 1975). Feeding activity shoed a slight increase through the period of the study ith anomalously high levels (as measured by both estimates of activity) during the last sampling period. (Tidal period did not appear to be related to feeding activity. ) The folloing considerations may serve, at least partially, to explain the feeding patterns: 1) certain species of phytoplankton may promote particularly high feeding rates; 2) higher temperatures incur greater energetic costs and hence may invoke greater feeding rates; 3) possible shock to colonies acclimated to the cold ambient temperatures of the Menai Straits early in the season (the suspension in the flo tank as at ambient laboratory temperature). Explanations 2 and 3, hoever, seem unlikely to explain the very dramatic difference in feeding activity beteen mid- and late July. > g.23 o (.) cr.21 Fig. 2. The mean ooid sie per colony from.. N early March to late.19 E July of 1985 (n = 5-47, colonies). Bars repre.17 sent 2 standard errors t! en about the mean. e.15 o N.13 Z «~.11 -F---+--M--+--A-l--M--+-J J-+- While the reasons for variation in feeding are unknon, the potential for such variation should be noted and accounted for in studies of bryooan feeding. In an earlier study (Okamura 1985) I noted a similar seasonal change in the feeding activity of colonies of Conopeum reticulum from San Francisco Bay, California. In that study activity levels ere higher earlier in the summer than later on. (Different experimental treatments ere run concurrently during the study, thus there as no problem in interpreting the results.)

5 SEASONAL CHANGES IN ZOOID SIZE AND FEEDING 21 Seasonal Patterns in Zooid Sie Sebens (1979) suggested that changes in the body sies of colonial suspension feeders may reflect changing food availability. He argued that if the prey sies become smaller or if food availability is high, it is advantageous for a single polyp (or ooid) of any sie to become to smaller polyps due to the concomitant increase in surface area for prey intake. The argument is based on the inverse scaling of surface area to volume. The data collected in this study appear to counter Seben's suggestion: larger ooids occurred at the time of peak primary productivity. Hoever, it is possible that some lag occurs before sie is expressed as a response to environmental influences. In addition, the measure of mean ooid sie reflected the mean sie of all oo ids in the colony, not just those that ere recently formed (see materials and methods section). Finally, since groth rates vary ith temperature (see belo), any lag beteen sie expression and environmental influence ill also vary temporally, making interpretation of a relationship in the data complex. While food availability may explain the sie changes observed in this study, I believe a stronger case can be made for temperatureinduction of ooid sie changes. Variation of body sie ith temperature and latitude appears to be a fundamental trait of both endotherms and ectotherms (e.g. Ray 196; Kinne 197; Mayr 197; Vermeij 1978; Nevo et al. 1986) although the mechanisms of temperature-mediated changes in body sie remain speculative. Postulated mechanisms include: 1) for endotherms, less heat ill be lost through radiation at larger body sies due to the inverse scaling of surface area to volume (commonly knon as Bergmann's Rule) (Mayr 1963: 319); 2) for ectotherms, increased rates of metabolism at high temperature reduce groth if energy intake is constant (Sebens 1982); 3) the observed attainment of larger cell sies at loer temperatures may produce organisms of larger body sie (Vermeij 1978); and 4) differentiation and sexual maturation may be more strongly temperature-dependent than somatic groth, thus delayed ontogeny may result in groth to large sie (Ray 196; Vermeij 1978). Experimental culture of bryooans further support a temperatureinduction of ooid sie changes (Menon 1972). Both Electra pilosa and Conopeum reticulum ere found to produce smaller oo ids at higher temperatures, although there as no significant sie change in ooids of Membranipora membranacea (Menon 1972). Hoever, as equal amounts of food ere provided, ooid sie changes may have reflected an energetic response: at higher temperatures the greater metabolic costs ma y have reduced ooid groth. Implications of Zooid Sie Changes Variation in ooid sie may occur both spatially, over latitudinal (Ryland 1963; Silen and Harmelin 1976; Morris 198) and possibly depth gradients (Popofsky, 198, cited in Kinne, 197, reported increased sies ith depth ~or radiolarians) and temporally, over seasonal (this paper) and annual cycles. Such variation is notable for several reasons. Care should be taken hen body sie is considered as a taxonomic character since there appears to be the potential for considerable temporal and spatial variation in ooid sie. In addition, changes in various dimensions of body sie are often used as morphological characters to measure evolutionary rates. The relative importance of evolutionary processes (e.g. phyletic gradualism vs. punctuated equilibrium)

6 22 BETH OKAMURA (Gould & Eldredge 1977) that influence rates of morphological change through geological time is a much-debated topic in evolutionary biology. To resolve this issue investigators have been studying biostratigraphic sequences for rates and patterns of morphological change (e.g. Dingus and Sadler 1982; Bell et al. 1985; Cheetham 1986). This study suggests that caution should be used hen employing body sie changes for the above arguments (see also Stanley 1985). Documented changes in body sie may not reflect true evolutionary change but rather may simply represent displacement of assemblages in space or time. ACKNOWLEDGEMENTS I ish to acknoledge the help and encouragement provided by Dr. R. Seed during my studies in North Wales. J. Pell aided in field collections and laboratory experiments. Dr. A.H. Cheetham encouraged me to report these findings, and conversations ith Dr. S. Lidgard clarified my thoughts. To all I am grateful. This is contribution no. 176 of the Smithsonian Marine Station at Link Port. REFERENCES AI-Hasan, R.H., S.J. Coughlan, Aditipant, & G.E. Fogg Seasonal variations in phytoplankton and glycolate concentrations in the Menai Straits, Anglesey. -J. mar. biol. Ass. U.K. 55: Bell, M.A., J.V. Baumgartner, & E.C. Olson Patterns of temporal change in single morphological characters of a Miocene stickleback fish. -Paleobiol. 11: Buchan, S., F.D. Floodgate, & D.J. Crisp Studies on the seasonal variation of the suspended matter in the Menai Straits. I. The inorganic fraction. -Limnol. Oceanogr. 12: Cheetham, A.H Tempo of evolution in a Neogene bryooan: Rates of morphologic change ithin and across species boundaries. -Paleobiol. 12: Coates, A.G. & J.B.C. Jackson Morphological themes in the evolution of clonal and aclonal marine invertebrates. -In J.B.C. Jackson, L.W. Buss & R.E. Cook (eds): Population biology and evolution of clonal organisms, pp Yale University Press, Ne Haven, Conn. Dingus, L. & P.M. Sadler The effects of stratigraphic completeness on estimates of evolutionary rates. -Syst. Zool. 31: Gordon, D.P Biological relationships of an intertidal bryooan population. -J. Nat. Hist. 6: Gould, S.J. & N. Eldredge Punctuated equilibria: the tempo and mode of evolution reconsidered. -Paleobiol. 3: Jackson, J.B.C Morphological strategies of sessile animals. -In G. Larood & B.R. Rosen (eds): Biology and systematics of colonial organisms, pp Academic Press, London. Jones, M. & C.P. Spencer The phy toplankton of the Menai Straits. -J. du Conseil 33: Kinne, O Marine ecology. Vol. 1. Part 1. Temperature. -Wiley Interscience, London. Lovett-Doust, L Population dynamics and local specialiation in a clonal perennial (Ranunculus repens). I. The dynamics of ramets in contrasting habitats. -J. Ecol. 69: Mayr, E Animal species and evolution. -Harvard University Press, Cambridge, Mass. Mayr, E Populations, species, and evolution. -The Belknap Press of Harvard University Press, Cambridge, Mass.

7 SEASONAL CHANGES IN ZOOID SIZE AND FEEDING 23 Menon, N.R Heat tolerance, groth and regeneration in three North Sea bryooans exposed to different constant temperatures. -Mar. Biol. 15: 1-1l. Morris, P.A The bryooan family Hippothoidae (Cheilostomata Ascophora) ith emphasis on the genus Hippothoa. -In Monograph Series of the Alan Hancock Foundation. No.1. Nair, N.B Ecology 'of marine fouling and ood boring organisms of estern Noray. -Sarsia 8: Nevo, E., A. Beiles, G. Heth & S. Simson Adaptive differentiation of body sie in speciating mole rats. Oecologia (Berl.) 69: Okamura, B The effects of ambient flo velocity, colony sie, and upstream colonies on the feeding success of Bryooa. II. Conopeum reticulum (Linnaeus), an encrusting species. -J. expo mar. Biol. Ecol. 89: Ray, C The application of Bergmann's and Allen's Rules to the poikilotherms. -J. Morph. 16: Ryland, J.S The species of Haplopoma (Polyoa). -Sarsia 1: Ryland, J.S Bryooans. -Hutchinson University Library, London. Sebens, K.P The energetics of asexual reproduction and colony formation in benthic marine invertebrates. -Am. Zool. 19: Sebens, K.P The limits to indeterminate groth: an optimal sie model applied to passive suspension feeders. -Ecol. 63: Seed, R., M.N. Elliot, P.J.S. Boaden, & R.J. O'Connor The composition and seasonal changes amongst the epifauna associated ith Fucus serratus L. in Strangford Lough, Northern Ireland. -Cah. Biol. mar. 22: Seed, R. & R.J. O'Connor Community organiation in marine algal epifaunas. -Ann. Rev. Ecol. Syst. 12: Silen, L. & J.-G. Harmelin Haplopoma sciaphilum sp.n., a caveliving Bryooan from the Skagerrate and the Mediterranean. -Zool. Scripta 5: Stanley, S.M Rates of evolution. -Paleobiol. 11: Stebbing, A.R.D Groth of Flustra foliacea (Bryooa). -Mar. Biol. 9: Taylor, P.D. & R.W. Furness Astogenetic and environmental variation of ooid sie ithin colonies of Stomatopora (Bryooa, Cyclostomata). -J. Paleontol. 52: Vermeij, G.J Biogeography and adaptation. Patterns of marine life. -Harvard University Press, Cambridge, Mass. Wood, V. & R. Seed The effects of shore level on the epifaunal communities associated ith Fucus serratus (L) in the Menai Strait, North Wales. - Cah. Biol. mar. 21:

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