4/5/2018

1

BIOLOGY AND ECOLOGY OF

CIGUATOXINS PRODUCERS

Chui Pin LEAW PHD

IOES, University of Malaya

Harmful benthic dinoflagellates

Coolia

Gambierdiscus

Ostreopsis

Prorocentrum

Fukuyoa

Amphidinium

4/5/2018

2

e.g. Yasumoto et al. 1979, 1987, 2005; Chambell et al. 1987; Chinain et al. 1999 and many more…

O u t l i n e

Taxonomy and biodiversity

Eco-physiology

4/5/2018

3

Gambierdiscus toxicus Adachi et Fukuyo 1979

Adopted from Adachi & Fukuyo 1979

Courtesy of J. Larsen Sousa & Silva 1956

4/5/2018

4

Taxonomic t imel ine

G. toxicus

1995

G. belizeanus

1979 1998 1999

G. polyneseinsis G. australes G. pacificus G. yasumotoi

1 decade ~2 decades

2009

G. caribaeus G. carpenteri

G. carolinianus G. ruetzleri

2011

2015 2016

2017

G. balechii G. cheloniae G. lapillus

G. honu G. ribotype 3

G. excentricus

2014

F. yasumotoi F. ruetzleri F. paulensis

G. scabrosus G. silvae

G. type 1 – 6

G. ribotype 1 – 2

Morphology-based Molecular-based

Species characterization

Culture establishment

Field specimens

Microscopic observation

4/5/2018

5

Molecular characterization

Sequence analysis

Species identified by comparing with library Flag new and/or cryptic species Gene amplifications

Phylogenetic and phylogeographic analyses

Genomic DNA isolation

Gambierdiscus Fukuyoa

C el l shapes

4/5/2018

6

Courtesy of J. Larsen

Plate tabulat ions

Leaw et al. 2011

4/5/2018

7

Leaw et al. 2011

(Mustapa et al. 2015)

Key to species

4/5/2018

8

Courtesy of J. Larsen

Courtesy of J. Larsen

4/5/2018

9

Alternative approach in monitoring - Molecular detection by quantitative PCR assay (qPCR)

Gambierdiscus sp. type 6 = Gambierdiscus balechii

(Dai et al. 2017 Harmful Algae)

4/5/2018

10

L i fe h istory

Bravo et al. 2014

Dividing cells were mostly in the cluster comprising the largest cells, indicating that mitosis takes place in diploid cells.

PHYSIOLOGICAL AND ECOLOGICAL ADAPTIONS OF CIGUATOXINS PRODUCERS

4/5/2018

11

Distr ibut ion

35 oN – 37 oS (Parson et al. 2012)

Adopted from Rhodes et al. 2017

4/5/2018

12

Temperature is the primary environmental factor regulating growth. Optimum T = ~25 – 31oC

phys iology

e.g. Bomber et al. 1988, Kibler et al. 2012, Xu et al. 2016

Eco-physio logy

Chinain et al. 1999

Cells reached maximum abundance at the beginning and the end of hot season.

e.g. Bomber et al. 1988, Bagnis et al 1990, Morton et al. 1992, Hokama et al. 1996, Chinain et al. 1999

Tahiti Island

4/5/2018

13

Chinain et al. 1999

Variability in toxin production may be due to the presence of multiple toxic species of Gambierdiscus.

Supported by studies of Litaker et al. (2017), Pisapia et al. (2017).

Irradiance >10 and <200-700 umol photons m-2 s-1

Low light requirement

phys iology

Salinity Stable, high salinity

4/5/2018

14

BHAB species

Species diversity?

Healthy coral reef

Degraded coral reef

Alteration of trophic transfer

Local stresses

Climate changes

Disturbance Frequency HIGH

Reef Recovery LOW

Algal palatability HIGH

CFP vector shift

Degraded reefs

4/5/2018

15

Chinain et al. 1999

Coral mass-bleaching event

660 824 866 924 CFP cases

Maximum cell abundance and toxin production

Coral morbidity may be the factor in the genesis of naturally-occuring blooms of Gambierdiscus spp. by providing “new surfaces” for colonization by opportunistic macroalgae that are ideal hosts for Gambierdiscus. Support the hypotheses

that CFP outbreaks can occur in response to disruption of reefs Time lag may be only a few months

Rongo & van Woesik (2011, 2013) Rarotonga, Cook Islands

Vector shift (1989-2000 > 2001-2005 > 2006-2009) Herbivore >> benthic invertivore/ bivalves >> herbivore & carnivore

4/5/2018

16

Non-destructive sampling approach

(Tester et al. 2012, 2014; Tan et al. 2013)

Reef surveys and sample collection

Underwater photoquadrat survey was performed at the sampling sites to record the percent coral coverage, variety of benthic substratum and the biotic inhabitants (e.g. fishes, invertebrates).

4/5/2018

17

Microalgae-habitat interactions

Coral rubbles overgrown with algal turf

G O C P A

(Yong et al. under reviewed)

Resource competition or allelopathic interaction may occur between Gambierdiscus and macrophytes

Algal turf

4/5/2018

18

(Yong et al. under reviewed)

Northeast monsoon (Wet season)

Southwest monsoon (Dry season)

Temporal variability

32.7 oC

30.0 oC

Cells were absent in wet season, the monsoonal events may shift the population into a successional phase and promoting recolonization at the onset of dry season. As cyst formation in Gambierdiscus has been documented, this life-history trait may be an adaptive strategy to overcome the unfavorable disturbance in the wet season and increase resilience of cells. This may be a good studied subject to prove the phenomenon. The population declined in mid of the year when water temperatures are at their hottest and the light intensity at the highest.

4/5/2018

19

Northeast monsoon (Wet season)

Southwest monsoon (Dry season)

Temporal variability

Ostreopsis temporal distribution displayed a manner opposite to that of Gambierdiscus. It reach maximum abundance in Jun, which is the hottest time of the year. It seems to withstand the harsh weather in the wet season, and perhaps the trait of ability to form massive mat is the advantage here.

Experiment on substrate/host preference

Gambierdiscus cultures

Collecting macroalgae

Experimental setup

Cell count

e.g. Parson et al. 2011, 2015

4/5/2018

20

Host preference of Gambierdiscus species

G. balechii showed higher growth rate in all algal treatment compared to other strains. Different species of Gambierdiscus exhibit different host preferences.

(Mustapa et al. in prep)

BHAB species generally occur at various bottom substrata (not strictly habitat-dependent), but dominating specific habitats with different ecological optima (i.e. temperatures, light, nutrients etc.).

It suggests a more complex ecological interactions of BHAB communities, and the species may possess different adaptive strategy to dominate specific microhabitats.

Understanding the traits and adaptations may provide insights into the mechanism driving the community along the changing influential variables

4/5/2018

21

4/5/2018

22