BENTHIC HARMFUL ALGAL BLOOMS - Stefano Accoroni Dipartimento di Scienze della Vita e dell'Ambiente, Università Politecnica delle Marche, Ismar-Cnr
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BENTHIC HARMFUL ALGAL BLOOMS
Stefano Accoroni
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche,
Ancona Italy
CNR ISMAR - Ancona, Italy, 16 January 2018.
Red tides / Harmful Algal Blooms
The expression ‘Red Tides’ is
unfortunate for several reasons
it is not a tidal phenomenon,
HABs may have different colours
when associated with water
discolouration,
shellfish toxicity may occur at
very low cell concentrations, i.e.
Harmful Algal Blooms It appears that HABs are spreading and increasing in intensity: • due to increased awareness of HABs • climate changes particularly increasing temperature • transportation and spreading of species in ship’s ballast water
Harmful Algal Blooms
Algal blooms can determine heavy consequences for the ecosystems and
for human activities.
Impact on human health (shellfish and fish poisoning, respiratory
problems, drinking water problem).
Karenia brevis – Florida, US
Human syndromes (PSP, DSP,
ASP, NSP, CFP, AZP, etc.) Microcystis
Harmful Algal Blooms
Algal blooms can determine heavy consequences for the ecosystems and
for human activities.
Impact on human economy (e.g. recreational resources, aquaculture).
Karenia - Hong Kong
Alexandrium taylori, Mallorca,Spain
Benthic Harmful Algal Blooms
Benthic microalgae grow on several
types of benthic substrata
(macrophytes, rocks, invertebrates,
sands) often forming a brownish,
mucilaginous mat that can be easily
resuspended in the water column.
Factors:
• Nutrients
• Temperature
• Light (depth)
• Hydrodynamics
• Substratum
Ostreopsis cf. ovata
Benthic Harmful Algal Blooms
Gambierdiscus
Ciguatera fish poisoning, the most frequent algal toxin-related
seafoodborne illness, is caused by ingestion of marine fish
contaminated with ciguatoxins produced by several Gambierdiscus
species.
Ciguateric fish poisoning
(CFP)
Algae Herbivorous fish Carnivorous fish
Benthic Harmful Algal Blooms
Gambierdiscus
Ciguatoxins are neurotoxins producing different symptoms
(gastrointestinal, bradycardia with hypotension, cold allodynia,
paresthesia, dysesthesia) that can last from weeks to months. Typical
of tropical regions.
Benthic Harmful Algal Blooms
Gambierdiscus
Recently, Gambierdiscus spp. has been documented in subtropical and
temperate latitudes.
Laza-Martínez et al., 2016
open triangles ciguatera poisoning cases
Benthic Harmful Algal Blooms
Prorocentrum
Diarrhetic Shellfish Poisoning is a gastrointestinal intoxication due to
ingestion of contaminated shellfish contaminated with okadaic acid
produced by several Prorocentrum species (among other genera).
Headache
Chills
Nausea
Vomiting
Diarrhea
Abdominal
pain
Digestive
tract
tumorsBenthic Harmful Algal Blooms
Prorocentrum
No. Species References
1. Prorocentrum arabianum Morton et Faust 2002 Morton et al. (2002)
2. P. arenarium Faust 1994 Faust (1994), Ten-Hage et. al. (2000)
3. P. belizeanum Faust 1993 Faust (1993a), Morton et al. (1998), Faust et al. (1999)
4. P. borbonicum Ten-Hague et al. 2000 Ten-Hague et al. (2000)
5. P. carribaeum Faust 1993 Faust (1993a)
6. P. clipeus Hoppenrath 2000 Hoppenrath 2000
7. P. concavum Fukuyo 1981 Fukuyo (1981), Faust et al. (1999), Taylor et al. (2004)
Several 8. P. donghaiense Lu et al. 2002 Lu et al. (2005)
Prorocentrum
9. P. elegans Faust 1993 Faust (1993a)
10. P. emarginatum Fukuyo 1981 Fukuyo (1981), Faust et al. (1999), Taylor et al. (2003)
species are 11. P. faustiae Morton 1998 Morton (1998)
benthic and
12. P. foraminosum Faust 1993 Faust (1993b), Faust et al. (1999)
13. P. formosum Faust 1993 Faust (1993b)
cosmopolitan (e.g. 14. P. hoffmannianum Faust 1990 Faust (1990), Faust et al. (1999), Taylor et al. (2004)
Prorocentrum
15. P. lima (Ehrenberg) Dodge 1975 Faust et al. (1999), Taylor et al. (2004)
16. P. maculosum Faust 1993 Faust (1993b), Faust et al. (1999)
lima). 17.
18.
P. mexicanum Osorio-Tafall 1942
P. norrisianum Faust 1997
Cortes-Altamirano & Sierra-Beltran (2003)
Faust (1997)
19. P. panamensis Grzebyk et al. 1998 Grzebyk et al. 1998
20. P. reticulatum Faust 1997 Faust (1997)
21. Faust et al. (1999) (as P. mexicanum), Cortes-Altami-rano & Sierra-
P. rhathymum Loeblich et al. 1979
Beltran (2003), Taylor et al. (2004)
22. P. ruetzlerianum Faust 1990 Faust (1990), Faust et al. (1999)
23. P. Sipadanensis Mohammad-Noor,
Mohammad-Noor et al. 2007
Daugbjerg et Moestrup 2007
24. P. consutum Chomérat et Nézan 2010 Chomérat et al. 2010
25. P. bimaculatum Chomerat et Saburova 2012 Chomérat et al. 2012
26. P. sabulosum Faust 1994 Faust (1994)
27. P. sculptile Faust 1994 Faust (1994)
28. P. tropicalis Faust 1997 Faust (1997)
29. P. vietnamensis Yoo et al. 2004 Yoo et al. (2004)Benthic Harmful Algal Blooms
Ostreopsis
Ostreopsis produce a large array of palytoxin analogues, i.e. isobaric
palytoxin, ovatoxins, ostreocin-D and mascarenotoxins, and
ostreotoxin. Ostreopsis blooms are associated with many cases of
• suffering or mass mortalities of various marine organisms
• human illness (e.g. fever, cough, dyspnea, sore throat, rhinorrhea,
skin irritation, etc.) attributed to inhalation or cutaneous contact
with cells or toxic aerosol.
• clupeotoxismBenthic Harmful Algal Blooms
OstreopsisBenthic Harmful Algal Blooms
Ostreopsis
3 species:
• Ostreopsis cf. ovata, O. cf. siamensis and O. fattorussoiOstreopsis fattorussoi Accoroni, Romagnoli & Totti
• O. fattorussoi produces OVTX-a and
structural isomers OVTX-d and –e, so far
found only in O. cf. ovata, and three
exclusive palytoxin-like compounds (OVTX-i,
OVTX-j1, OVTX-j2, and OVTX-k).
• Toxin content of O. fattorussoi was in the
range of lower (0.06–0.94 pg cell−1) than
that of a Mediterranean O. cf. ovata (up to
44.0 pg cell−1).
Accoroni et al., 2016, Journal of PhycologyCase study:
Blooms of Ostreopsis cf. ovata
Photo: Dr. Di CioccioStudy area
Passetto
ANCONAMethods
• Study period: 2007-2015 from June to
November
• Frequency: 15 dd before and 5-7 dd after 1st cell
appearance Ulva rigida
• Sampling of undisturbed substrata:
• macroalgae (3 replicates)
• pebbles (3 replicates)
• water column (1 replicate) Dictyota dichotoma
• Environmental parameters: T, S, meteomarine
conditions, nutrients (3 replicates)
Hypnea
Hypneamusciformis
musciformisMethods
• Treatment of substrata to obtain
the complete removal of Ostreopsis
cells.
• Substrata measurements:
• Thalli → fw, dw, area
• Rocks → area
• Identification, counting and
measurements at inverted light
microscope.
• PCR analysis to confirm
morphological identification.
• Toxin analyses: samples were
filtrated (< 5 mbar) to separate cell
pellets from seawater. Abundances
• Statistical analysis: ANOVA, Tukey expressed as
test •cells g-1 fw
•cells g-1 dw
•cells cm-2Temporal trend and relationship with T
• N Adriatic Sea • Ligurian, Tyrrhenian, S Adriatic
Seas
• Appearance: Aug
• Appearance: June
• Peak: in late summer (Sep-Oct)
• Peak: summer (Jul-Aug)
• Decline: end Oct/early Nov
• Decline: Sep
Max abundances at decreasing T Max abundances at max T
From Totti et al. 2010 Harmful Algae From Mangialajo et al. 2008 Mar. Poll. Bull.Relationships with temperature
A trigger role of temperature may be hypothesized, as cyst germination
occurs only at T=25 °C in experimental conditions.
T=25 °C
Vegetative cells
Double-walled cysts Accoroni et al., 2014, Harmful AlgaeRelationships with nutrients
2009
• Adriatic Sea high P limitation.
• Ostreopsis optimal N:P ratio: ~ 16
(Vanucci et al., 2012; Vidyarathna 2010
and Granéli, 2013)
• PO4 concentrations were
significantly higher in bloom onset
than in either bloom maintenance 2011
phase or the pre-bloom conditions
(p < 0.01)
2011
Accoroni et al., 2015,
Harmful Algae
• DIN: 2.391-17.338 µmol l-1
• PO4: 0.008-0.324 µmol l-1The bloom onset: temperature and nutrients
2009 2011
2010 2012
Accoroni et al., 2015, Harmful Algae
• T threshold of 25 °C germination of cysts
Bloom onset
• N:P ratio around Redfield cell proliferationRelationships with hydrodynamics
E
S
20 Passetto S 20
Passetto E
avg macroalgae avg macroalgae
cells cm -2 10 3
15 15
cells cm -2 10 3
10 10
5 5
0 0
9-Apr
6-Oct
6-Oct
9-Apr
7-Aug
6-Sep
7-Aug
6-Sep
24-Apr
21-Oct
21-Sep
21-Oct
24-Apr
22-Aug
22-Aug
21-Sep
8-Jul
8-Jun
8-Jul
8-Jun
9-May
9-May
25-Mar
23-Jul
23-Jul
23-Jun
24-May
25-Mar
24-May
23-Jun
• Abundances were significantly higher in sheltered than in exposed
sites (Totti et al., 2010, Harmful Algae; Accoroni et al., 2012, Harmful
Algae).Relationship with depth
Abundances were significantly higher at depths < 3m than at depths > 3m
(p < 0.05), likely related to light availability.
Totti et al., 2010, Harmful AlgaeRelationship with substrata 2007 2009 Totti et al., 2010, Harmful Algae Accoroni et al., 2011, Mar. Pollut. Bull. Abundances on rocks were significantly higher than those on macroalgae suggesting that living substrata allow lower concentration of epibionts than any other substrate, probably due to the production of some hypothetical allelopathic compounds.
Relationship with substrata
Accoroni et al.,2015b HA
In laboratory, all the investigated seaweeds [Dictyota dichotoma (brown
alga), Rhodymenia pseudopalmata (red alga) and Ulva rigida (green alga)]
exerted negative effects toward Ostreopsis growth.Conceptual diagram
Pre-bloom A Pre-bloom B Bloom onset C Bloom D
maintenance
+P
N:P N:P N:P N:P
N:P
Accoroni et al., 2015, Harmful Algae Mixotrophy?Mixotrophic nutrition
Accoroni et al. 2017,
Water research
The increase in phosphatase activity coincided with the start of
proliferation phase, lasting until the bloom decline .Mixotrophic nutrition
Accoroni et al. 2017, Water research
BCIP-NBT staining showed PMEase activity was closely associated with
cells, located both extracellularly and intracellularly.Mixotrophic nutrition
Accoroni et al., 2017, Water research
The ability of Ostreopsis to use organic P source explain why
Ostreopsis is able to thrive in low P environments.Toxin production
Harmful dinoflagellates are generally known to change their toxin
production with stress related to the variations of several factors
Granéli et al.
2008 HA
Nutritional stress → increase toxin production to fight competitors
and grazers, and aiding mixotrophy.Toxin production
Vanucci et al., 2012, HA
Both laboratory and field studies
highlighted that those conditions that
led to the bloom start are the same that
likely maximize the toxin production.
Ostreopsis showed a gradual decrease
of toxin content toward the bloom
decline.
Accoroni et al.,
2017, MPBToxin production
Nutritional stress → increase toxin production to fight competitors
and grazers, and aiding mixotrophy.
Accoroni et al., 2017, MPB
Ostreopsis is promptly able to fight both competitors and grazers,
resulting in a very successful bloom start.Toxin production
• The microphytobenthos
community showed a
significant lower value of
Shannon diversity index
during the presence of
Ostreopsis cf. ovata
than in the rest of the
year.
• Several benthic diatoms
can produce PUAs able
to reduce the
Ostreopsis growth
(Pichierri et al., 2016,
2017).
Accoroni et al., 2016b, Harmful AlgaeAcknowledgements
Collaborators
Cecilia Totti, Tiziana Romagnoli, Salvatore
Pichierri, Stefania Gorbi, Francesco Regoli,
Funding
Federica Colombo, Angela Pastore, Giacomo
Ciampi, Nicolé Caputo, Eleonora Antonucci • PRIN 2007, MURST,
(DISVA, UNIVPM) Ministry for University and
Scientific and Technological
Mauro Marini, Alessandra Campanelli (CNR Research
ISMAR Ancona)
• ISPRA-Italian Ministry of
Patricia Glibert (University of Maryland) Environment
Antonella Penna (University of Urbino) • ENPI CBCMED M3-HABs
project
Carmela Dell’Aversano (University of
Naples)You can also read
