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 rootsOxygen translocated from the leaves is released into the sediments

Nutrient uptake by leaves and rootsOxygen 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?

Zertuche et al., 2009

2004

Introduction

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 translocatedNutrient fluxes reduced

Introduction

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient fluxes reduced

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient fluxes reduced

Increase of amonium and sulfide.Hypoxia

Introduction

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient fluxes reduced

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient fluxes reduced

Increase of amonium and sulfide.Hypoxia

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient fluxes reduced

Increase of amonium and sulfide.Hypoxia

Short shoots are immersed in toxic concentrations. Anoxia

Introduction

Green macroalgae shade seagrasses

Decrease of oxygen translocatedNutrient 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

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

Objetive and Hipothesis

Irradiance, temperature, sampling site

Guano

Defoliation

Algal blooms

Defoliation x Guano

Guano x Algae

Defol x Algae x Guano

Defol. x Algae

Objetive and Hipothesis

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

Per seagrass bed (site):

1. No treatment

2. Cut of leaves (C)

3. Ulva addition (U)

4. Nutrient enrichment (N)

5. C x U

6. C x N

7. U x N

8. C x U x N

9. Control PVC (K)

n=4, one sample per site

Materials and Methods

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 SamplingNon destructive response variables. Monthly

Materials and Methods

Field SamplingNon destructive response variables. Monthly

Seagrass and algal cover and seagrass density (5)

Materials and Methods

Field SamplingNon destructive response variables. Monthly

Leaf length (10)

Materials and Methods

Field SamplingNon destructive response variables. Monthly

Epiphytes cover (5)

Materials and Methods

Field SamplingNon destructive response variables. Monthly

C and N content

January(0.001 m2) (1)

March (from biomass; 3)

Materials and Methods

Field SamplingDestructive response variables. March 2008

Aboveground biomass (3)

Belowground biomass (3)

Materials and Methods

Laboratory Work

Monthly samples

•Epiphytes cover: Armitage et al. (2005)0 = absent0.1 = one individual < 5% cover0.5 = few individuals < 5 % cover1 = many individuals < 5% cover2 = 5-25% cover3 = 25-50% cover4 = 50-75% cover5 = 75-100% cover

Materials and Methods

Laboratory Work

Biomass samples

AlgaeZostera

roots

Leaves

Clean and freeze-dry

clean

dry

weight

C:N

epiphytes leaves

%C

Materials and Methods

Data Treatment

1.- New variables from data:

• Z. marina growth: monthly increase in total stem length (density x leaf length)

C = (Lt+1-Lt)/Lt*100

• % N, %C and C:N increase: I = (VJanuary-VMarch)/VMarch*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)

Materials and Methods

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 siteMarch warmer (F=48.92; p < 0.01)

Upwelling in March 16th 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

Abo

vegr

ound

b.

(g m

-2)

Bel

owgr

ound

b.

(g m

-2)

Results

C=clipped; U=Ulva; N=nutrient

C CN CU CUN K N U UN0

10

20

30

40

50

60

C CN CU CUN K N U UN50

100

150

200

250

300

350

Mean ± SE

Effects of Treatments on Z. marinaA

bove

grou

nd b

. (g

m-2)

Bel

owgr

ound

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

C CN CU CUN K N U UN0

10

20

30

40

50

60

C CN CU CUN K N U UN50

100

150

200

250

300

350

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

January M arch2,5

2,6

2,7

2,8

2,9

3,0

% N

No Ulva Ulva

3

2.9

2.8

2.7

2.6

2.5

Mean ± SE

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

N o v -D e c D e c -Ja n Ja n-F e b F e b -M a r-1 0 0

0

1 0 0

2 0 0

3 0 0

Relative G

rowth (cm

)

N o c l ip p e d C l ip p e d

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

N o v -D e c D e c -Ja n Ja n-F e b F e b -M a r-1 0 0

0

1 0 0

2 0 0

3 0 0

Relative G

rowth (cm

)

N o c l ip p e d C l ip p e d

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 herbivoryThis 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

% c

ove

r

Bio

mas

s (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

% c

ove

r

Bio

mas

s (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.

Dec Jan Feb M ar0

1

2

Cover Index

N o c l ip p e d C l ip p e d

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

C CN CU CUN K N U UN0

1

2

3

4

5

6

7

8

9

Epiphyte B

iomass (g m

-2) Pneophyllum confervicola

Results

C=clipped; U=Ulva; N=nutrient Mean ± SE

Dec Jan Feb M ar0

1

2

Cover Index

N o c l ip p e d C l ip p e d

Effects of Treatments on Epiphytes

C CN CU CUN K N U UN0

1

2

3

4

5

6

7

8

9

Epiphyte B

iomass (g m

-2) 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

Z. marina R2 Irradiance Green algae Site 1 Site 2 EpiphytesAbovegroun B. 0.848 -24.39 -17.61 -15.39 12.72 62.67Belowground B. 0.444 -0.499 -0.11 0.178

Density 0.842 -246.28 -194.47 294.01Leaf Length 0.56 10.312 -10.36 8.44

# leaves 0.499 -0.071 -0.04

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

AgradecimientosGracias 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