1. Jose Abella Gutiérrez Comité Dra. Silvia E. Ibarra Obando Dra. Theresa Sinicrope Talley Dra. Sharon Herzka Llona Dr. Stephen Vaughan Smith Efectos de la herbivoría de las brantas y los florecimientos algales en la comunidad de Zostera marina

2. Jose Abella Gutiérrez Comité Dra. Silvia E. Ibarra Obando Dra. Theresa Sinicrope Talley Dra. Sharon Herzka Llona Dr. Stephen Vaughan Smith Effects of Brant Herbivory and Algal Blooms on Zostera marina Community

3. Introduction

4. Introduction Seagrasses as Engineers

5. Introduction DETRITIC PATHWAY Chesapeake Bay Seagrasses as Engineers

6. Valentine, J.F., y Heck, Jr., K.L., 1999 . Seagrass herbivory: evidence for the continued grazing of marine grasses. Mar. Ecol. Prog. Ser., 176: 291-302. Introduction

7. Valentine, J.F., y Heck, Jr., K.L., 1999 . Seagrass herbivory: evidence for the continued grazing of marine grasses. Mar. Ecol. Prog. Ser., 176: 291-302. Turtles and Sirenians are important in some systems. Change in herbivorous species. There are others grazers (limpets, sea urchins, fish, waterfowl). Seagrass is food Introduction

8. Branta bernicla nigricans Ward et al., 2005 Introduction

9. Branta bernicla nigricans Ward et al., 2005 Introduction Moore et al., 2004 Ward et al., 2005

11. Herbivory Effects on Seagrass Architecture “ Since defoliation by grazers rarely kills the host plant, it is generally believed that the principal effect of herbivory is to reduce the competitiveness of grazed individuals rather than to cause outright mortality” (Hulme, 1996) Seagrass Macroalgae Epiphytes Microphytobenthos Phytoplancton Fauna Introduction

12. Herbivory Effects on Nutrient Cycling Introduction Thayer et al., 1982

20. Ward et al., 2003 Bahía Falsa; Oct – 2007 Eelgrass decline in favor of green macroalgae. Increase of herbivory intensity as a consequence? Introduction Zertuche et al., 2009 2004

21. Burkholder et al 2007 Seagrass Eutrophication Introduction

23. Introduction

24. Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Introduction

25. Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Increase of amonium and sulfide. Hypoxia Introduction

26. Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Increase of amonium and sulfide. Hypoxia Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Increase of amonium and sulfide. Hypoxia Short shoots are immersed in toxic concentrations. Anoxia Introduction

27. Green macroalgae shade seagrasses Decrease of oxygen translocated Nutrient fluxes reduced Increase of amonium and sulfide. Hypoxia Short shoots are immersed in toxic concentrations. Anoxia Plant dies and bed disappears if conditions persist Introduction

28. Objective: Understand plant-herbivory interactions in seagrasses with frequent and continual algal blooms Hypothesis: Interactions between algal blooms and herbivory will produce a quick shift from seagrass to algal beds Objetive and Hipothesis

29. Objetive and Hipothesis Guano Defoliation Algal blooms

30. Objetive and Hipothesis Guano Defoliation Algal blooms Defoliation x Guano Guano x Algae Defol x Algae x Guano Defol. x Algae

31. Irradiance, temperature, sampling site Objetive and Hipothesis Guano Defoliation Algal blooms Defoliation x Guano Guano x Algae Defol x Algae x Guano Defol. x Algae

32. Materials and Methods

33. Manipulative experiment from Nov-07 to Mar-08 4 seagrass beds: continuous beds, same depth Materials and Methods

34. Treatment Simulations Clipped treatment (2 cm, 3 months): No differences between plots RM-ANOVA F(6, 14)=0.123, p=0.99 Fertilizer addition Multicote Ulva addition Materials and Methods

35. Treatment Simulations Clipped treatment (2 cm, 3 months) Fertilizer addition Multicote: DIN: 23.6 (± 6.9) g/mes DIP: 8.6 (± 2.5) g/mes Ulva addition Materials and Methods

36. Treatment Simulations Clipped treatment (2 cm, 3 months) Fertilizer addition Multicote Ulva addition: 2 Kg wet weight 0.876 (± 369.4) Kg Materials and Methods

38. Fully Factorial Experimental Design Using Randomized Complete Blocks Materials and Methods

39. Field Sampling Materials and Methods 3 underwater thermistors in 3 sites from Nov 07 to Mar 08 1 light sensor from Nov 07 to Mar 08 5 light sensors during last month (4 sites + land)

40. Field Sampling Materials and Methods Non destructive response variables. Monthly

41. Field Sampling Materials and Methods Non destructive response variables. Monthly Seagrass and algal cover and seagrass density (5)

42. Field Sampling Materials and Methods Non destructive response variables. Monthly Leaf length (10)

43. Field Sampling Materials and Methods Non destructive response variables. Monthly Epiphytes cover (5)

44. Field Sampling Materials and Methods Non destructive response variables. Monthly C and N content January(0.001 m2) (1) March (from biomass; 3)

45. Field Sampling Destructive response variables. March 2008 Materials and Methods Aboveground biomass (3) Belowground biomass (3)

47. Laboratory Work Materials and Methods Biomass samples Algae Zostera roots Leaves Clean and freeze-dry clean dry weight C:N epiphytes leaves %C

49. Data Analysis 3-way ANOVA destructive samples 3-way Repeated Measures ANOVA monthly variables MRA: Z. marina ~ site, light, Tª, green algae, brown algae and epiphytes Materials and Methods

50. Results and Discussion

51. Enviroment: Irradiance Data from 10 am to 2 pm Feb-Mar standardized irradiance (site/land): ANOVA: F = 17.59; p < 0.001 Tukey: C B D A Site B Results Mean ± SE

52. Environment: Temperature and Upwelling Temperature : 2-way ANOVA, month and site March warmer (F=48.92; p < 0.01) Upwelling in March 16 th Bakum index = 296 m -3 s -1 Results

53. Effects of Treatments on Z. marina Aboveground and belowground biomass were reduced in plots with clipped treatment 3-ANOVA: F = 16.4, p <0.001; F = 10.26, p < 0.01 Aboveground b. ( g m -2 ) Belowground b. ( g m -2 ) Results C=clipped; U=Ulva; N=nutrient Mean ± SE

54. Effects of Treatments on Z. marina Aboveground b. ( g m -2 ) Belowground b. ( g m -2 ) Discussion Study Aboveground Belowground Valentine and Heck, 1999 40-50% 40-50% Nacken and Reise, 2000 47 % 43% Rivers and Short, 2007 100% This study ~ 70% ~ 40% C=clipped; U=Ulva; N=nutrient Mean ± SE

55. There was no effect of treatments on Z. marina %N, %C or C:N per month %N decreased from January to March except when Ulva treatment was involved (3 way ANOVA: F=5.51, p <0.05) Results Effects of Treatments on Z. marina Mean ± SE 3 2.9 2.8 2.7 2.6 2.5

56. Results Discussion Study: (%N or C:N) Aboveground Belowground Vergés et al., 2008 0=1=3 > 2 0>1>2>3 McGlathery, 1995 no differences Ibarra-Obando et al., 2004 no differences Ferson, 2007 no differences This study no differences Effects of Treatments on Z. marina

57. Large seasonal variability (cover, density, # leaves) Clipped treatment affected cover and density Results Effects of Treatments on Z. marina C=clipped; U=Ulva; N=nutrient Mean ± SE

58. Cut treatment enhances growth RM-ANOVA: F=6.01, p <0.01 Results Effects of Treatments on Z. marina Mean ± SE

59. Discussion Decrease or increase in density? C = [( D *L) t+1 - ( D *L) t ] / ( D *L) t * 100 Density was reduced DURING treatment but increased AFTER treatment Effects of Treatments on Z. marina Mean ± SE

60. Discussion Decrease or increase in density? C = [( D *L) t+1 - ( D *L) t ] / ( D *L) t * 100 Density was reduced DURING treatment but increased AFTER treatment GROWTH shoots leaves Moran and Bjorndal, 2005 X Vergés et al., 2008 X Valentine et al., 1997 X Hughes and Stachowicz, 2004 X Ferson, 2007 X X This study X X Ferson, 2007: moderate herbivory > control > high herbivory This study: very high herbivory > control Effects of Treatments on Z. marina Mean ± SE

61. Discussion Seagrasses regrew after 3 events of simulated herbivory in 60 days. Seagrasses disappeared with 3 – 6 herbivory events (Valentine and Heck, 1991, 1999; Heck and Valentine, 1995; Maciá, 2000) Ulva addition can reduce seagrass biomass and production (Hauxwell et al., 2001) and density (Nelson and Lee, 2001), but not in this experiment Unsuccessful enrichment Effects of Treatments on Z. marina

62. Discussion There was no synergistic effect of algal blooms and herbivory (defoliation) on eelgrass Maciá, 2000: Interactions between urchin defoliation and macroagal blooms on Thallasia testudinum density but not on biomass Effects of Treatments on Z. marina

63. Seasonal influence on brown algae cover No significant differences between treatments Effects of Treatments on Green and Brown Macroalgae % cover Biomass (g m -2 ) Results March C=clipped; U=Ulva; N=nutrient. Z. marina ; Green A.; Brown A.

64. Effects of Treatments on Green and Brown Macroalgae % cover Biomass (g m -2 ) Discussion High variability : Ulva clathrata, U. expansa and Dyctiota undulata are floating macroalgae Presence of upwelling during March March C=clipped; U=Ulva; N=nutrient. Z. marina ; Green A.; Brown A.

65. Large seasonal influence on epifaunal, green and red algae cover. Clipped treatment affected total biomass, but not its relationship with Z. marina. Also affected red algae cover Effects of Treatments on Epiphytes Pneophyllum confervicola Results C=clipped; U=Ulva; N=nutrient Mean ± SE

66. Effects of Treatments on Epiphytes Pneophyllum confervicola Discussion Settlement of epiphytes in less than 14 days (Borum, 1987) Differences in settlement patterns across groups (Borowitza et al., 1990) C=clipped; U=Ulva; N=nutrient Mean ± SE

67. Effects of Enviroment on Eelgrass Characteristics Irradiance, green algae biomass, site and epiphyte biomass were related with some Z. marina characteristics Results

69. Conclusions Large seasonal and spatial variability Simulated herbivory affected eelgrass, but seagrass reserves allowed the recovery of the bed The decrease in Z. marina aboveground biomass produced a parellel decrease in epiphyte biomass Although no effect of Ulva on eelgras was found, there was a negative relationship between green macroalgae and eelgrass

70. Future investigations It is necessary separate herbivory effects during grazing and after grazing More research is needed to understand the relationship of N content in seagrasses and grazing preferences by herbivores More studies of eutrophication are needed in estuaries affected by upwelling More research that explores the interactions between algal blooms and herbivory is necesary

71. Agradecimientos Esta tesis corresponde a los estudios realizados con una beca otorgada por la Secretaría de Relaciones Exteriores del Gobierno de México. El trabajo fue financiado por el proyecto de UC-MEXUS 622-215 (O0C053): Efecto de las brantas sobre las comunidades de pastos marinos en Bahía de San Quintín

72. Agradecimientos Gracias a mi comité A Drew Talley A Juan Guerrero y Ana Salazar A Hector Atilano y Miriam Poumian A Victor Camacho y Pepe Zertuche A los hermanos Aguilar A aquellos que me acompañaron al campo voluntariamente: Tiago, Doris, Marta, Annelise, Vania, Daniela, Lluis, Berta, Julian, Mariana, Yuca, Karla, Brenda, Luis, Mónica y Tomás. Así como a los trabajadores de San Quintín que nos echaron una mano para cortar el “zacate marino” A aquellos que me ayudaron en el laboratorio voluntariamente o en servicios sociales. Entre otros, Elsa, Araceli, Venecia, Raul y Filipo. Que ahora no recuerde los nombres de algunos de ellos no significa que les esté menos agradecido. A Gabi Y a toda la gente de CICESE...

73. Muchas gracias por demostrarme que uno puede sentirse como en casa incluso en el extranjero