Effects of Guano Page 2 Abstract Gigartina papillata (Rhodophyta) cultured in high con- centrations of NO, NH, and guano for 10 days showed the same changes in R-phycoerythrin for all three conditions. G. papillata from an area with high guano exposure off China Point on the Monterey Peninsula showed significantly (p.01) more phycoerythrin and significantly (pc.05) less carrageenan than control sites with little guano exposure. G. papillata was also shown to be significantly (p£.01) thicker in distal branches than in control sites. Endocladia muricata (Rhodophyta) and G. papillata from high guano density areas were shown significantly (p£.01) shorter and had significantly (p.01) less branching than did the same species in control sites. Effects of Guano Page 3 Introduction In coastal waters, there are various types of con¬ centrated sites of animal waste of which several examples are seal and sea lion rookeries, human sewage outfalls and guano deposits produced by birds. Algal marine communities effected by seal excrement has been investigated (Hanson, Judy 1971: Hanson, John 1972). Although the bulk of most research is on sewage effluent produced by humans, there has been some mention in the literature on the effect of shore bird guano. Guano has been implicated in enhancing the production of phytoplankton as well as enhancing the production of fish (Wheeler 1945). But on the whole, there have been no systematic attempts to détermine what the consequences of this excretory product are. Questions such as does this nitrogen and phosphorous rich compound produce a favorable environment for local organisms? or does this substance act more as a pollutant than as a nutrient? or are there no effects at all? have never been adequately answered. In this paper, I discuss the differences in Gigartina papillata and Endocladia muricata between areas with intense guano exposure and guano free areas and I present experimental evidence which implicates guano as a factor in causing some of these differences. Effects of Guano Page 4 Materials and Methods The study site consisted of a group of rocks approx¬ imately fifty meters off China Point on the Monterey Penin- sula (see figure 1.) At the time of the study, these rocks supported a large population of seagulls, approximately twenty cormorants, two oyster catchers, and a few transient pelicans. All sampling within the study site was done along a 20 meter transect, running parallel to the coast- line, on the protected side of Bird Rock. The control sites with relatively little guano exposure consisted of areas 1 and 2 in figure 1. Random numbers were generated corresponding to a 20 meter transect and at each point samples of algae were obtained from the control site and from the study site. Samples were taken from approximately three feet above the mean lower tide level. Length is the distance between the frond origin at the holdfast to the tip. Branching is the number of branch points radiating from the stipe. Thickness for G. papillata only, was determined by measur- ing the mid portion, with a micrometer, of the most distal branch of the holdfast origin. R-phycoerythrin was extracted from G. papillata samples in 6 ml. of .025 Tris-HCl per .4 g. ground dry algae sample. Each sample was extracted for four hours at five degrees after which maximum absorption at 565 nm. (Siegelman et al. 1978) using a model DU Beckman spectrometer. Effects of Guano Page 5 Total carrageenan content was determined by a method recommended by E. L. McCandless in personal communication and modified by Huskins (personal communication). The algae used were male or sterile G. papillata from the study site and from the control sites. Each sample was dried, ground in a ball mill, and then weighed portions of about 1.5 g. were added to 200 ml. of distilled water with 5 ml. of 2% NaOH. After extraction at 80-90 degrees centigrade for 18 to 22 hours, the samples were filtered with celite and the fil¬ trate was added to 2.5 times its volume of isopropyl alcho¬ hol to precipitate the carrageenans which were subsequently filtered, dried and weighed. Guano and non-guano G. papillata were cultured in various concentrations NH,, NO., PO, and guano. Refer to table 1. Solutions were changed every three days and were under constant aeriation and were grown outside in constant day/night cycles. The temperature was kept constant in a constantly circulating seawater bath. A portion of the plant was used to est- ablish initial phycoerythrin levels. Ten days later at the termination of the experiment final absorption was determined. Results Figures 2A and 2B show the differences in length and the amount of branching between the study site and control site 2 in E. muricata and G. papillata. Using the student's t-test, the guano plants were found to be significantly (pc.01) shorter and have significantly (p£01) less branching. Effects of Guano Page 6 Figure 3A depicts the differences between G. papillata distal frond thickness from guano and non-guano areas. Guano G. papillata were shown to be significantly (p£.01) thicker than non-guano G.papillata. Figure 3B depicts the differences in R-phycoerythrin content between guano and non-guano plants. Guano G. papillata were found tohave significantly (p2.01) more phycoerythrin. Figure 4 depicts the carrageenan content as a percentage of dry weight in guano and non-guano G. papillata. Non- guano algae were shown to have signifieantly (p7.05) more carregeenan than guano algae. The results of the growth experiment are presented in figure 5. No appreciable increase in phycoerythrin was exhibited in any of the conditions. NH, and guano both had the same effect in decreasing the phycoerythrin content in the study site plants. However, the control and PO, condition decreased the absorption to a greater extent than guano or NH,. In the non-guano algae, NH,, NO, and guano had the same effect in maintaining the phy¬ coerythrin content constant. In the control condition, the phycoerythrin content decreased. Discussion High guano exposure does produce quantifiable dif¬ ferences in algae growth as demonstrated by the data. Shacklock, et al. (1975) have shown that carrageenan production is inversely related to the amount of available Effects of Guano Page 7 nitrogen. In the presence of nitrogen, proteins are prefer¬ entially produced. As the nitrogen levels drop, protein production is suppressed and the excess carbons are stored in the form of such polysacharrides as carregeenans. The low levels of carregeenan in the guano area algae indicates that there has been nitrogen enrichment. Phycorythrin is a protein bound accesory photopigment primarily responsible for the color of red algae (Abbott, Hol¬ lenberg 1976). The high phycoerythrin in plants near guano (see figure 3B) was sufficient to make them obviously darker in color. Pigment concentration increases with increasing nitrogen levels (Eocha 1965); the high levels of this pig- ment in the study site relative to the control site indicate a high nitrogen concentration. There were deviations from what was expected. Study site plants when grown in guano and NH, decreased in pigment content instead of staying the same or increasing; appreciable increases did not occur in control site algae grown in NH,, NO, or guano. These discrepancies could be attributed to a nitrogen defficiency in all conditions and particularily in the ambient and phosphate situations. Or more concievably, the environment in an erlenmeyer flask is not ideal for optimal growth. There is a positive correlation between the amount of carrageenan and the ability to resist desiccation (Huskins 1979). If carrageenan is instrumental in preventing desic¬ cation in the high intertidal zone of the study site, G. papil- lata containing small amounts of carrageenan would seem to be maladapted for survival. Effects of Guano Page 8 The guano plants have a smaller surface to volume ratio than the carrageenan rich control plants being shorter, thicker and less branched. These morphological traits may have developed as a means of compensating for a relative lack of carrageenan in combatting a deadly desiccation at low tide. Conclusions (1) This study showed that there were quantifiable differences between guano and non-guano areas and that these differences could be attributed to guano. (2) Figure 8 summarizes the conclusions that can be drawn from this study. As nitrogen and guano levels increase phycoerythrin content rises while carrageenan con¬ centrations drop. This investigation underscores the ability of biological (3) organisms to adapt to a variety of environmental conditions. Through their morphological changes, plants residing in high guano exposed areas have been able to respond successfully to an environmental stress. Effects of Guano Page 9 Literature Cited Abbott, I. A. and Hollenberg, G.J. 1976. Marine Algae of California. Stanford University Press, Stanford Hanson, John 1972. Marine algal nutrient regeneration: the enrichment of water surrounding Ano Nuevo Island California by pinnipeds. Masters Thesis, Fresno State College, 47 pp. Hanson, Judy 1971. Effects of pinniped excreta on marine benthic algae of Ano Nuevo Island California. Masters Thesis, Fresno State College, 74 pp. Huskins, C. 1979. The relation of carrageenan content and dessication resistance to tidal height in Gigar- tina papillata. Unpublished. Hopkins Marine Station, Pacific Grove, California. O hEocha, C. 1965. Chemistry and biochemistry of plant pigments. In: Lewin (editor), Physiology and Bio¬ chemistry of Algae. Academic Press, London, pp. 421-435. Provasoli, L., McLaughlin, J. J. A., and Droop, M. R. 1957. The development of artificial media for marine algae. Arch. Mikrobiol. 25: 392-428 Shacklock, P. F., Robson, D. R., and Simpson, F. J. 1975 Vegetative propagation of Chondrus crispus (Irish Moss) in tanks. Technical Report No. 21 of the Atlantic Regional Laboratory, National Research Council of Canada, Halifax, N. S. Siegelman, W., and Kycin, J. H. 1978. Algal biliproteins. In: Hellebust and Craigie (editors), Hand Book of Effects of Guano Page 10 Phycological Methods, Cambridge University Press, London, pp. 72-78 Wheeler, W. M. 1945. Plant nutrients in the sea. Nature, Vol. 155, pp. 731-732 Page 11 Effects of Guano Acknowlegements I would like to express sincere gratitude for the effort and time William Magruder spent on minenand every¬ one else's projects. I would also like to thank Judy Hanson for her insights and suggestions. Special apprecia¬ tion goes to Robin Burnett for showing me that Biology in the field could be as exciting as Biology in the class¬ room. Effects of Guano Page 12 Figure Legends Figure 1: China Point on the Monterey Peninsula. Study site and control sites 1 and 2 are shown. Figure 24: Differences in length between guano and non-guano algae. Standard errors are shown by the vertical bars. Figure 2B: Differences in the number of branches between guano and non-guano algae. Figure 3A: Frond thickness for G. papillata between guano and non-guano areas. Vertical bars show standard errors. Figure 3B: Changes in absorption between guano and non-guano G. papillata. Vertical bars show standard errors. Figure 4: Differences in carrageenan content as a percentage of dry wieght between guano and non-guano G. papillata. Figure 5: Results showing initial and final absorption of G. papillata grown in various nutrient concentrations. Figure 6: Percentage of initial phycoerythrin after ten days growth in various nutrient conditions in guano and non¬ guano G. papillata. Figure 7: The relationship between nitrogen, guano, phycoery- thrin and carrageenan is depicted. e a §0 § 0 o S E d O 5 a ac Z . :.. ..: 8 Effects of Guano Length — o X Number of Branches o a 3ko- Page 14 — Effects of Guano Thickness of Frond Absorption — Page 15 0 Page 16 Effects of Guano percentage carrageenan 8 k l 1 Effects of Guano Page 17 Absorption oo 8 — — a- Effects of Guano % of Initial Absorption So OE Effects of Guano Phycoerythrin Carrageenan Page 19 Effects of Guano + Page 20 0 8