Déjà Vu All Over Again: The Impact of Recent Cyanobacteria Blooms on Hard-bottom Communities in Florida Bay and the Florida Keys

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1 Déjà Vu All Over Again: The Impact of Recent Cyanobacteria Blooms on Hard-bottom Communities in Florida Bay and the Florida Keys Mark Butler Old Dominion University, Norfolk, Virginia Don Behringer University of Florida, Gainesville, Florida

2 Nearly Two Decades Ago ( ) A Cascade of Disturbances in Florida Bay Changes in Water Quality Cyanobacteria Bloom Seagrass Die-off Impacts on Crevice-dwelling Fauna (e.g. Lobster) Sponge Die-off

3 Sponge Die-off Studies by My Colleagues & I Documented changes in sponge community structure Documented changes in juvenile lobster population structure, shelter use, & recruitment Hypothesized ecological linkages: blooms sponges lobster Photo Credit: Rod Bertelsen

4 When one tugs at a single thing in nature, one finds it attached to the rest of the world. - John Muir

5 Our Subsequent Research on Hard-bottom 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

6 Déjà Vu A Cascade of Disturbances in Florida Bay 2007 Changes in Water Quality Cyanobacteria Bloom Seagrass Die-off Impacts on Crevice-dwelling Fauna (e.g. Lobster) Sponge Die-off

7 Hard-bottom Monitoring: Sites 132 sites in 2002; sites in Methods surveyed annually in June/July 4 permanent 2 x 25m transects/site 16 permanent 1m 2 quadrats/site Measurements Abundance of 55 taxa (24 spp. sponge) Size structure selected sponges & octocorals Lobster population structure & disease 2002 Only

8 Pre-bloom & Post-bloom Surveys 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 N Survey locations 10 km

9 2007 Bloom Impacts on Sponges Severe Impacts - 22 of 24 sponge species killed Loggerhead sponges: 100% Vase sponges: 100% Commercial sponges: 100% Other sponges: 90% N Survey locations 10 km

10 2007 Bloom Impacts on Sponges Severe Impacts Moderate Impacts Loggerhead sponges: 67% Vase sponges: 90% Commercial sponges: 95% Other sponges: 50% N Survey locations 10 km

11 2007 Bloom Impacts on Sponges Severe Impact Moderate Impact Little or No Impact N Survey locations 10 km

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17 Vulnerability of Sponge Species (Percentage of each species killed on bloom-impacted sites) Cinachyra sp. Niphates erecta Speciospongia vesparia Ircinia sp. Adocia sp. Tethya crypta Tedania ignis Chondrilla nuclea Ircinia campana Halichondria melandocia Aplysinia sp. Lissodendoryx sp. Haliclona/Geodia Aaptos sp. Anthosigmella varians Hytrios sp. Hippospongia lachne Ircinia felix Spongia graminea Spongia cheris Spongia barbara % Killed Mean + 1sd Most Tolerant Least Tolerant

18 Survivors

19 Mechanism of Sponge Die-off? Mechanical Inhibition of Filtration? Sponge filtration efficiency varies among seasons and species Sponge filtration efficiency declines precipitously at bloom cell densities (Peterson & Fourquerean) Most Tolerant Cinachyra sp. Niphates erecta Speciospongia vesparia Ircinia sp. Adocia sp. Tethya crypta Tedania ignis Chondrilla nuclea Ircinia campana Halichondria melandocia Aplysinia sp. Lissodendoryx sp. Haliclona/Geodia Aaptos sp. Anthosigmella varians Hytrios sp. Hippospongia lachne Ircinia felix Spongia graminea Spongia cheris Spongia barbara Least Tolerant % Killed % Bacteria Removed Mean + 1sd Summer Winter Less Efficient More Efficient N = 5-20 Golfball Sheepswool Yellow Vase Glove Loggerhead Branching The more efficient sponge species are the least tolerant of blooms, especially in summer when blooms typically develop

20 Consequences of Sponge Die-off 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 Following the 1991 die-off:... we calculated that prior to the sponge die-off the sponge community could filter the water column every 3d. In contrast, it would now take 15d for the surviving sponge community to do the same. (Peterson et al 2006)

21 Consequences of Sponge Die-off Loss of Sponge Infaunal Animal Communities Large sponges harbor within their internal canals a variety of macroinvertebrates Some are obligate sponge-dwellers, including the only known eusocial marine animals (snapping shrimp) Zuzalpheus spp. Photo credit: D. Rubenstein

22 Consequences of Sponge Die-off Loss of Sponge Infaunal Animal Communities Change in hard-bottom community sound-scape Unimpacted Sites Sponge Die-off Sites

23 Consequences of Sponge Die-off Loss of Shelter for Crevice-dwelling Animals (e.g., Juvenile Spiny Lobster) Shelter use & aggregation Abundance Nutritional condition Disease Juvenile lobsters sheltering under sponge Photo credit: Rod Bertelsen Lobster hemocytes infected with PaV1 virus Photo credit: Jeff Shields

24 Consequences of Sponge Die-off Aggregation of Juvenile Spiny Lobster comparison of impacted & unimpacted sites after sponge die-off Frequency Lobster Den Occupancy Post Sponge Die-off Unimpacted Sites (n = 12) Impacted Sites (n = 13) >10 Number of Lobsters / Den

25 Consequences of Sponge Die-off Aggregation of Juvenile Spiny Lobster time series at two sites before & after sponge die-off Mean No. Lobsters / Den Unimpacted Site: Burnt Point Sponge Die-off Impacted Site: KOA Sponge Die-off 0 July 1999 May 2000 April 2001 June 2001 Oct 2007 Mar 2008 July 1999 May 2000 April 2001 June 2001 Oct 2007 Mar 2008

26 Photo Credit: Rod Bertelsen

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28 Fewer sponges creates larger lobster aggregations but does this also lead to higher prevalence of PaV1 disease due to increased contact transmission? Behringer, Butler & Shields Nature 2006 Frequency Shelter Competition Experiment: 1 Diseased Lobster 3 Healthy Lobsters 2 shelters N = Diseased Lobster Alone Diseased & Healthy Together

29 Sponge Die-Off Impacts on Lobster sites % Lobsters Injured Hemolymph Protein Index % Visibly Diseased (PaV1) Abundance 13 sites 12 sites Size Den Sharing 0 means + 1 sd Disease 13 sites Nutrition Injuries Number of Lobsters / Shelter Lobster Size (mm CL) Lobster Abundance (CPUE) Unimpacted Impacted Unimpacted Impacted

30 Spiny Lobster / Sponge Spatially Explicit IBM Model Spatial Structure of Individual-Based Spiny Lobster Recruitment 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 Individual-based Population Dynamics 28 Day Loop Day Loop Effect of cyanobacteria blooms & sponge die-off on lobster recruitment Settlement Growth Emigration Aggregation in juvenile lobsters: an examination of the group defense & guide-post hypotheses empirically-based probability functions daily time step for each individual in model for specified number of yrs Mortality Shelter Selection (e.g. ~ 10 million individuals in a 10 year simulation) PaV1 Disease

31 Summary Impact of blooms on hard-bottom communities appears to be similar to that in , although bloom genesis is different Sponge die-off widespread in middle Florida Keys (~ 200 km 2 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

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