Nutrient loading & benthic
native-invasive species dynamics
Romberg Tiburon Center Seminar Series5 November 2008
Heidi W. Weiskel & Edwin D. Grosholz
University of California, DavisRomberg Tiburon Center (adopted)
Cerithidea californica Ilyanassa obsoleta
Global Increase in Nitrogen
Effects of Eutrophication
Threats to Coastal Ecosystems
Global Increase in Invasions
Conceptual Framework
Global Increase in NitrogenHowarth et al. 1996
The substantial nitrogen increase has “caused changes in the composition and functioning of estuarine and nearshore ecosystems, and contributed to long-term declines in coastal marine fisheries.”(Vitousek et al. 1997)
Nitrogen a Concern in Marine Systems
• N-limited
• Change algal &
plant community
• Can create
hypoxic (<2 mg O2/L)
or anoxic (<0 mg O2/L)
zones
• Change herbivore, predator, ¶site behavior
(food web impacts)
http://library.thinkquest.org/04oct/01590/pollution/culturaleutroph.jpg
Effects of Eutrophication
http://www.marietta.edu/~biol/biomes/images/mangroves/florida_eutrophication_7536.jpg
http://cache.eb.com/eb/image?id=90452&rendTypeId=4
• As trade increases, biological invasions are
increasing in both terrestrial and aquatic
ecosystems (Levine & D’Antonio 2003)
• “One of the five most critical environmental
issues facing the ocean’s marine life” (NRC 1995)
Global Increase in Invasions
– Nutrients can facilitate invasion success(Pennings et al. 2005, Tyler et al. 2007)
• increase productivity
• increase biomass, even with increased herbivory
– Invasive plants can edge out their competitors(Ehrenfeld 2003, Fargione et al. 2003, Levine et al. 2003)
• capable of fixing nitrogen
• partition nutrient resources
Plant Nutrient-Invasion Dynamics
Would we expect the effects of nutrients to propagate up to higher trophic levels?
Animal-Nutrient Invasion Dynamics
Atlantic mud snail Ilyanassa obsoleta
Talk Outline
• Conceptual framework for research
• Introduction to system in San Francisco Bay
• Nutrient-invasion experiments
• 2007 results & conclusions
• 2008 preliminary results
• Future Directions
Estuaries highly invaded compared to outer coast (Wasson et al. 2005)
Cohen & Carlton 1998
Estuaries disproportionately vulnerable to nutrient
pollution & eutrophication (Bricker et al. 1999, Anderson et al. 2002)
Cloern 2001
SAN FRANCISCO BAYInvasions Nutrients
Robert’s Landing - >
San
Francisco Bay, CA
Inspiration
Photo Credit: J.T. Carlton
Ilyanassa obsoleta Cerithidea californica
Omnivore/Deposit Feeder Herbivore / Deposit Feeder
Introduced 1907 Native
30 mm
Previous Studies
• Northern CA work:
invasive successfully
competes with &
disturbs the native (Race 1982)
• Southern CA work:
native does not
influence microalgae
but is negatively
affected by nutrients(Armitage & Fong 2004)
Can nutrients alter competitive
dynamics between native and invasive
consumers in a marine system?
Cyanobacteria
IlyanassaCerithidea
DiatomsO2
Trophic Dynamics
MUD
NUTRIENTS
Objectives
• Test the direct effects of nutrients on consumers
• Investigate the impacts of nutrients on the competitive dynamics between native & invasive consumers
• Further our understanding of the effects of nutrients in invaded, eutrophic intertidal systems
Hypotheses1) The invasive snail will be POSITIVELY affected by nutrients
Nutrients Diatoms Cyanobacteria Growth Mortality
2) The native snail will be NEGATIVELY affected by nutrients
Nutrients Diatoms Cyanobacteria Growth Mortality
Experimental DesignFactor I = Snail Density (7) Factor 2 = Nutrients (2)
No Cage Control
0 Density Cage
0 Invasive 50 Native
50 Invasive 0 Native
No Nutrient Additions
Nutrient Additions
0 Invasive 100 Native
100 Invasive 0 Native
50 Invasive 50 Native
C
L
H
Response Variables
Snail populations– Growth– Mortality
Microalgal community– Composition (HPLC)– Density (Microscopy & chl a)
Habitat characteristics– Organic matter– Grain size– Carbon-nitrogen ratios– Stable isotopes– Nutrients (ammonium)
Field Experiment 2007
2 nutrient events4,800 snails96 cages
Nutrients Influence the Effects of Grazing
by the Invasive Snail
0
100
200
300
400
500
NoSnails
Native
Open M
udBoth
Spp
Inva
sive
Snail Treatment
Fu
co
xa
nth
in l
ev
els
(u
nc
on
ve
rte
d)
Fertilized
Unfertilized
NS NS
No
Cage
p < 0.05p = 0.07
p = 0.09
= 50 Invasive snails
= 50 Native snails
No
Snails
Nutrients Influence the Effects of Grazing
by the Invasive Snail
0
100
200
300
400
500
NoSnails
Native
Open M
udBoth
Spp
Inva
sive
Snail Treatment
Fu
co
xa
nth
in l
ev
els
(u
nc
on
ve
rte
d)
Fertilized
Unfertilized
NS
No
Cage
p < 0.05
= 50 Invasive snails
= 50 Native snails
No
Snails
Growth Increases With Nutrients
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
Low
Nat
ive
Hig
hNat
ive
BothN
ativ
e
Low
Inva
sive
Hig
hInv
asiv
eBot
hInv
asiv
e
Density Treatments
Gro
wth
(m
m)
Fertilized
Unfertilized
* p < 0.0001 Fert/Unfertacross all density treatments
NATIVE
**
*
p = NS Fert/Unfertacross all density treatments
No Growth Increase With Nutrients
INVASIVE
Density Treatments
Fertilized
Unfertilized
0.00
0.50
1.00
1.50
2.00
2.50
3.00
3.50
4.00
Gro
wth
(m
m)
Nutrients Reduce Mortality At High Snail
Density
0
10
20
30
40
50
60
Low
Den
_Nat
ive
Hig
hDen
_Nat
ive
Both_
Nat
ive
Low
Den
_Inv
asH
ighD
en_I
nvas
Both_
Inva
s
Density Treatments
Perc
en
t M
ort
ali
ty (
%)
Fertilized
Unfertilized
**
NATIVE
**
** p < 0.005 Fert/Unfertacross all density treatments
Nutrients Reduce Mortality At High Snail
Density
0
10
20
30
40
50
60
Low
Den
_Nat
ive
Hig
hDen
_Nat
ive
Both_
Nat
ive
Low
Den
_Inv
asH
ighD
en_I
nvas
Both_
Inva
s
Density Treatments
Perc
en
t M
ort
ali
ty (
%)
Fertilized
Unfertilized
INVASIVE
**
** p < 0.005 Fert/Unfertacross all density treatments
Expectation for the invasive snail:nutrients diatoms cyanobacteria growth mortality
Outcome for the invasive snail:nutrients diatoms cyanobacteria growth mortality
N/A
Expectation for the native snail:nutrients diatoms cyanobacteria growth mortality
Outcome for the native snail:nutrients diatoms cyanobacteria growth mortality
N/A
2007 Conclusions
The invasive snail negatively affects the native snail � resource competition
Nutrients increase growth & reduce mortality in the native snail & reduce mortality in the invasive snail
� nutrients ameliorate stressful conditions
SF Bay benthic habitats can be nutrient-limited
� contrary to existing paradigm
Native response to nutrients is positive & strong
� Other factors?
Nutrient effects may be habitat-dependent
Nutrients increase food qualityand ameliorate stressful conditions
in nutrient-limited systems
Original Habitat Preferences
N
I
I
N
N = Native I = Invasive
Spartina eradication opened new habitat
Both Species Found at Higher Densities in Transition Zone
0
20
40
60
80
100
120
140
160
180
Low Mudflat High Marsh Transition Zone
Habitat
Nu
mb
er
of
Sn
ail
s (
pe
r s
q m
)
Invasive
Native
0
2
4
6
8
10
12
14
16
18
High Low Outfall
Tidal Elevation
Invasive
Native
Sediment
Stable Isotope Analysis Reveals Differences
between Species & Habitats
NS * * = p < 0.05
between species
Predation Pressure• Lab trials with invasive green crab Carcinus
• Field anecdotal evidence
– Low marsh cages only
Snail Mortality from Carcinus Predation
0
50
100
Ilyanassa Cerithidea
Snail Species
Pe
rce
nt
Mo
rta
lity
Percent Mortality
Field Experiment 2008
5 nutrient events9,600 snails168 cages
2008 Results to DateDiverse microalgal community
Modified habitat use
General Conclusions
• The overall effects of nutrients are habitat-dependent– Increase edible microalgal biomass and quality (higher N)– Facilitate competitive advantage for toxic cyanobacteria
• The overall effects of invaders are negative– Invasive snail outcompetes native snail (within trophic levels)
– Invasive crab preys on native snail only (between trophic levels)
• Nutrient effects on invaders vary
– Ameliorate effects of invaders in nutrient-limited systems (2007)
– Exacerbate effects of invaders in nutrient-replete systems (2008?)
Global Increase in Nitrogen
Effects of Eutrophication
Threats to Coastal Ecosystems
Global Increase in Invasions
Conceptual Framework
Future Steps• Test results with other species
– New snail invader Batillaria attramentaria
• Test results in other systems with different nutrient limitations– Cuba
– Southeast USA
• Introduce climate change into these study systems: How will increasing pCO2 and T interact with nutrients and invaders?– Productivity– Herbivory
– Predation
Special Thanks to Everyone at
RTC!!!• Dennis
• Chahn
• Brita
• Toby
• Kathy
• Jonathon
• Wim
• Sarah
• Tomoko
• Jaime
• Lara
• Anne
• Toni
• Raman
• Ed
• Chris B
• Dave
• Steph
• Gwen
• Lindsay
• Matt
• Chris R
• Chela
• Al
Acknowledgements• Advisor
Ted Grosholz
• Funding
• Lab Space & Equipment
• Volunteers & AssistantsChristy Bowles, Bryan Bugler, Andy Chang, Katie Faulkner, Stephanie Kiriakoplos, Stephen Lau, Sarah Lewis, Alice Lemeux, Nathan Mineo, April Ridlon, Gwen Santos, Jeffrey Waters, Betsy Wells, & Christine Whitcraft
APRIL!!!
Winter sunset in San Francisco Bay
QUESTIONS?