Mark ButlerOld Dominion University, Norfolk, Virginia

Don BehringerUniversity of Florida, Gainesville, Florida

Déjà Vu All Over Again: The Impact of Recent Cyanobacteria

Blooms on Hard-bottom Communities in Florida Bay and the Florida Keys

Nearly Two Decades Ago (1991-1992)A Cascade of Disturbances in Florida Bay

Changes inWater Quality

Seagrass Die-off

CyanobacteriaBloom

Sponge Die-off

Impacts onCrevice-dwelling

Fauna(e.g. Lobster)

• Documented changes in sponge community structure

• Documented changes in juvenile lobster population structure,shelter use, & recruitment

• Hypothesized ecological linkages: blooms → sponges → lobster

1991-1992 Sponge Die-off Studies by My Colleagues & I

Photo Credit: Rod Bertelsen

“ When one tugs at a single thing in nature,one finds it attached to the rest of the world.”

- John Muir

Monitoring of Hard-bottom

Sponge Research:• Population dynamics (growth, reproduction, recruitment)

• Tolerances for salinity, temperature& water quality correlations

• Filtration rates & particle selectivity• Sponge fishery effects

Modeling:• Salinity & bloom impacts on lobster recruitment and sponge/octocoral community structure

Our Subsequent Research on Hard-bottom

Déjà VuA Cascade of Disturbances in Florida Bay 2007

Changes in Water Quality

Seagrass Die-off

CyanobacteriaBloom

Sponge Die-off

Impacts onCrevice-dwelling

Fauna(e.g. Lobster)

Hard-bottom Monitoring: 2002 - 2007Sites• 132 sites in 2002; 32 -40 sites in 2003-2007

Methods• surveyed annually in June/July• 4 permanent 2 x 25m transects/site• 16 permanent 1m2 quadrats/site

Measurements• Abundance of 55 taxa (24 spp. sponge)• Size structure selected sponges & octocorals• Lobster population structure & disease

2002 - 20072002 Only

Pre-bloom & Post-bloom Surveys 2007 -2008

Survey locations

N

10 km

• 18 sites chosen from the central region of our hard-bottom monitoring program survey sites

• Hard-bottom surveys: July 2007 & Oct 2007• Lobster surveys: July 2007, Mar 2008, & July 2008

2007 Bloom Impacts on Sponges

Survey locations

N

10 km

Severe Impacts- 22 of 24 sponge species killed

Loggerhead sponges: ↓ 100%Vase sponges: ↓ 100%Commercial sponges: ↓ 100%Other sponges: ↓ 90%

2007 Bloom Impacts on Sponges

Survey locations

N

10 km

Moderate ImpactsSevere Impacts

Loggerhead sponges: ↓ 67%Vase sponges: ↓ 90%Commercial sponges: ↓ 95%Other sponges: ↓ 50%

2007 Bloom Impacts on Sponges

Survey locations

N

10 km

Moderate ImpactSevere Impact

Little or No Impact

% Killed0 20 40 60 80 100 120 140

Spongia barbaraSpongia cheris

Spongia gramineaIrcinia felix

Hippospongia lachneHytrios sp.

Anthosigmella variansAaptos sp.

Haliclona/GeodiaLissodendoryx sp.

Aplysinia sp.Halichondria melandocia

Ircinia campanaChondrilla nuclea

Tedania ignisTethya crypta

Adocia sp.Ircinia sp.

Speciospongia vespariaNiphates erecta

Cinachyra sp.

Mean+ 1sd

Vulnerability of Sponge Species(Percentage of each species killed on bloom-impacted sites)

MostTolerant

LeastTolerant

Survivors

• Sponge filtration efficiency varies among seasons and species

• Sponge filtration efficiency declines precipitously at bloom cell densities(Peterson & Fourquerean)

Mechanism of Sponge Die-off?

% B

acte

ria R

emov

ed

0

20

40

60

80

100

GolfballLoggerhead

SheepswoolBranching

Yellow Vase Glove

SummerWinter

N = 5 - 20

• The more efficient sponge species are the least tolerant of blooms,especially in summer when blooms typically develop

% Killed0 20 40 60 80 100 120 140

Spongia barbaraSpongia cheris

Spongia gramineaIrcinia felix

Hippospongia lachneHytrios sp.

Anthosigmella variansAaptos sp.

Haliclona/GeodiaLissodendoryx sp.

Aplysinia sp.Halichondria melandocia

Ircinia campanaChondrilla nuclea

Tedania ignisTethya crypta

Adocia sp.Ircinia sp.

Speciospongia vespariaNiphates erecta

Cinachyra sp.

Mean+ 1sd

Least Tolerant

Most Tolerant

More EfficientLessEfficient

Mechanical Inhibition of Filtration?

Loss of Filtration Capacity in System• Sponges are largest & most abundant

(biomass) filter feeders in this ecosystem

Per hectare: 4410 large sponges (>20cm dia)289,000 small sponges

• Sponges efficient consumers bacteria-sized particles; often > 80% particle removal efficiency

Consequences of Sponge Die-off

Following the 1991 die-off:“... we calculated that prior to the sponge die-off the sponge community could filter thewater column every 3d. In contrast, it would now take 15d for the surviving sponge community to do the same.”

(Peterson et al 2006)

Loss of Sponge Infaunal Animal Communities

• Large sponges harbor within their internal canals a variety of macroinvertebrates

Consequences of Sponge Die-off

Photo credit: D. Rubensteinwww.biology-blog.com/images

Zuzalpheus spp.

• Some are obligate sponge-dwellers, including the only known eusocial marine animals (snapping shrimp)

Loss of Sponge Infaunal Animal Communities

• Change in hard-bottom community “sound-scape”

Consequences of Sponge Die-off

Unimpacted Sites

Sponge Die-off Sites

Loss of Shelter for Crevice-dwelling Animals (e.g., Juvenile Spiny Lobster)

Consequences of Sponge Die-off

• Shelter use & aggregation• Abundance• Nutritional condition• Disease

Juvenile lobsters sheltering under spongePhoto credit: Rod Bertelsen

Lobster hemocytes infected with PaV1 virusPhoto credit: Jeff Shields

Consequences of Sponge Die-off

Number of Lobsters / Den1 2 3 4 5 6 7 8 9 10 >10

Freq

uenc

y

0

10

20

30

40

50

Unimpacted Sites (n = 12)Impacted Sites (n = 13)

Lobster Den Occupancy Post Sponge Die-off

Aggregation of Juvenile Spiny Lobster• comparison of impacted & unimpacted sites after sponge die-off

Consequences of Sponge Die-offAggregation of Juvenile Spiny Lobster• time series at two sites before & after sponge die-off

Mea

n N

o. L

obst

ers

/ Den

0

2

4

6

8

July1999

May2000

April2001

June2001

Oct2007

Mar2008

July1999

May2000

April2001

June2001

Oct2007

Mar2008

Unimpacted Site: Burnt Point Impacted Site: KOA

SpongeDie-off

SpongeDie-off

Photo Credit: Rod Bertelsen

Fewer sponges creates larger lobster aggregations …but does this also lead to higher prevalence of PaV1

disease due to increased contact transmission?

Freq

uenc

y

0

5

10

15

20

DiseasedLobster Alone

Diseased & HealthyTogether

N = 20

Shelter Competition Experiment: 1 Diseased Lobster3 Healthy Lobsters

2 shelters

Behringer, Butler & Shields Nature 2006

Sponge Die-Off Impacts on Lobster

% V

isib

ly D

isea

sed

(PaV

1)

0

5

10

15

20

25

Hem

olym

ph P

rote

in In

dex

0

5

10

15

20

% L

obst

ers

Inju

red

0

5

10

15

20

25

means + 1 sd

12 sites

13 sites

Num

ber o

f Lob

ster

s / S

helte

r

0

1

2

3

4

5

6

7

Lobs

ter A

bund

ance

(CPU

E)

0

10

20

30

Lobs

ter S

ize

(mm

CL)

0

10

20

30

40

50

60

13 sites12 sites

Unimpacted Impacted Unimpacted Impacted

Abundance

Den Sharing

Disease

Nutrition

Injuries

Size

Spatial Structure of Individual-Based Spiny

Lobster Recruitment Model

Individual-based Population Dynamics

MortalityMortalityMortalityMortality Shelter SelectionShelter SelectionShelter SelectionShelter Selection

GrowthGrowthGrowthGrowth EmigrationEmigrationEmigrationEmigrationSettlementSettlementSettlementSettlement

28 Day Loop Day Loop

PaV1 Disease

• empirically-basedprobability functions

• daily time step for eachindividual in model forspecified number of yrs

(e.g. ~ 10 million individualsin a 10 year simulation)

Spiny Lobster / SpongeSpatially Explicit IBM Model

Applications Thus Far:

• Everglades restoration: the effect of changing salinity on lobsters, sponges, & octocorals (in progress)

• Effect of a pathogenic virus and interactions with environmental change on lobster recruitment (in progress)

• Effect of spatial structure of nursery habitat • and postlarval supply on recruitment

• Effect of cyanobacteria blooms & sponge die-off on lobster recruitment

• Aggregation in juvenile lobsters: an examination of the group defense & guide-post hypotheses

Summary

• Impact of blooms on hard-bottom communities appears to be similar to that in 1991-1992, although bloom genesis is different

• Sponge die-off widespread in middle Florida Keys (~ 200 km2

area) and full recovery will take decades if no further blooms

• Sponge tolerance may be related to species-specific difference in filtration efficiencies?

• Ecosystem filtration capacity and habitat structure is greatly diminished in impacted areas, with a cascading loss of infaunal animals and crevice-dependent taxa, such as juvenile spiny lobster

• Lobster behavior appears to forestall increases in disease transmission expected in shelter-limited environment