Tesis Maestría

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

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

Introduction

Introduction Seagrasses as Engineers

Introduction DETRITIC PATHWAY Chesapeake Bay Seagrasses as Engineers

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

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

Branta bernicla nigricans Ward et al., 2005 Introduction

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

Herbivory Effects on Seagrass
Change in seagrass architecture
Guano enrichment and “shortcircuiting” of the detritus cycle
Introduction

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

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

Nutrient uptake by leaves and roots
Oxygen translocated from the leaves is released into the sediments
Nutrient uptake by leaves and roots
Oxygen translocated from the leaves is released into the sediments
Herbivory
Decrease of seagrass competitiveness
Increase of light and nutrients available for primary producers
Decrease of epiphytic abundance
… and usually seagrasses regrow!
Introduction

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

Burkholder et al 2007 Seagrass Eutrophication Introduction

Nutrient over-enrichment produces high biomass algal overgrowth
Seagrasses shaded by macroalgae
Unfavorable biogeochemical alterations
Seagrass Eutrophication Introduction

Introduction

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

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

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

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

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

Objetive and Hipothesis Guano Defoliation Algal blooms

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

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

Materials and Methods

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

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

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

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

Fully Factorial Experimental Design Using Randomized Complete Blocks Materials and Methods
Per seagrass bed (site):
No treatment
Cut of leaves (C)
Ulva addition (U)
Nutrient enrichment (N)
C x U
C x N
U x N
C x U x N
Control PVC (K)
n=4, one sample per site

Fully Factorial Experimental Design Using Randomized Complete Blocks Materials and Methods

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)

Field Sampling Materials and Methods Non destructive response variables. Monthly

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

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

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

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

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

Laboratory Work
Monthly samples
Epiphytes cover: Armitage et al. (2005)
0 = absent
0.1 = one individual < 5% cover
0.5 = few individuals < 5 % cover
1 = many individuals < 5% cover
2 = 5-25% cover
3 = 25-50% cover
4 = 50-75% cover
5 = 75-100% cover

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

Data Treatment
1.- New variables from data:
Z. marina growth : monthly increase in total stem length (density x leaf length)
C = (L t+1 -L t )/L t *100
% N, %C and C:N increase : I = (V January -V March )/V March *100
Primary producer / Z. marina (i.e. Epiphytes biomass / Z.marina biomass)
2.- No treatment and PVC control plots were merged = control
3.- Standardization (treatment / control)

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

Results and Discussion

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

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

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

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

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

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

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

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

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

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

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

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

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.

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.

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

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

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

GREEN ALGAE:
ANOVA: addition of Ulva did not affect Z. marina biomass
MRA: Negative relationship between Ulva and Z. marina biomass
Review (Young, 2009):
Worlwide: 32 studies, 29 reported eelgrass decline
Pacific Northeast: 4 studies, 2 reported effects on eelgrass
Algal bloom in San Quintin (Jan – Feb 2009) produced eelgrass decline but regrew (Jul – 09)
High resistance of seagrasses to change (i.e. Sfriso et al., 1989; Venice lagoon)
Discussion Effects of Enviroment on Eelgrass Characteristics

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

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

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

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...

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

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Tesis Maestría

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