Harmful algae. BIO 4400/ Bente Edvardsen

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1 Harmful algae Harmful algal blooms and their effects Harmful algae in the sea (and in fresh water) Algal toxins and their effects and symptoms Fish-killing algal blooms Monitoring of harmful algae BIO 4400/ Bente Edvardsen

2 Harmful algal blooms Algal blooms: Increased phytoplankton biomass due to rapid growth and accumulation One or a few species may become dominating Most algal blooms are non-harmful and beneficial Phytoplankton are primary producers

3 Algal blooms can colour the water red or brown, called red and brown tides The dinoflagellate Dinophysis spp. and the ciliate Myrionecta rubrum Bloom of the dinoflagellate Karenia mikimotoi Some blooms are harmful for animals and humans

4 Noctiluca scintillans heterotrophic dinoflagellate Luminescence (morild) Not all red tides are harmful

5 Blooms of cyanobacteria in fresh water Akersvannet, Vestfold Kolbotnvannet

6 Harmful algal blooms 3 types 1. Non-toxic, but high biomass cause harmful effects 2. Produce toxins that accumulate in the foob web. Harmful for humans on consumption of shellfish and fish. 3. Usually non-toxic for humans, but toxic for fish and some other animals

7 Toxic mussels and fish Harmful effects Health effects in humans upon consumption or other exposures Drinking water toxic for humans and animals Mass mortalities of fish and other aquatic organisms High biomass, noxious scum and smell lead to reduced quality of recreational areas Economic losses

8 Human health effects About 300 persons die every year of algal poisonings Thousands of people (>50 000) are poisoned every year and obtain long lasting negative effects

9 Economical losses for the aquaculture industry The algal catastrophe, Skagerrak, May 1988 Skagerrak 28 March 2001

10 Harmful algae in the sea Algal class BLÅGRØNNALGER (Cyanophyceae) In Norway Potentially toxic in Norway Nodularia spumigena FUREFLAGELLATER (Dinophyceae) SVEPEFLAGELLATER (Prymnesiophyceae) KISELALGER (Bacillariophyceae) NÅLFLAGELLATER (Raphidophyceae) KISELFLAGELLATER (Dictyochophyceae) Alexandrium tamarense Alexandrium ostenfeldii Dinophysis acuminata Dinophysis acuta Dinophysis norvegica Karenia mikimotoi Protoceratium reticulatum Azadinium spinosum Chrysochromulina polylepis C. leadbeateri Prymnesium parvum Heterosigma akashiwo Pseudochattonella farcimen Alexandrium minutum Prorocentrum minimum Prorocentrum lima Chrysochromulina spp. Pseudo-nitzschia multiseries P. seriata P. calliantha Olistodiscus lutheus Dictyocha speculum About 2% (ca 100 of 5000) of the marine microalgae are potentially toxic or harmful

11 Harmful algae in the sea Haptophytes (Svepeflagellater ) Photo Karl Tangen Prymnesium Photo Wenche Eikrem Chrysochromulina Protoceratium Alexandrium Dinoflagellates, fureflagellater Photo Lars Naustvoll Pseudochattonella Silicoflagellates (kiselflagellater) Karenia Dinophysis

12 Toxigenic cyanobacteria in Norwegain lakes Order Species Toxin Type of poisoning Chroococcales Microcystis aeruginosa Polypeptides Hepatotoxic Microcystis botrys Delayed effect Snowella lacustris other Woronichinia naegeliana Nostocales Anabaena lemmermannii Polypeptides Hepatotoksisk Anabaena flos-aquae Alkaloides Neurotoxic Anabaena circinalis Unknown Delayed effect Anabaena solitaria other Anabaena planctonica Anabaena crassa Anabaena tenericaulis Aphanizomenon flos-aquae Oscillatoriales Planktothrix agardhii Polypeptider Hepatotoksisk Planktothrix rubescens Alkaloider Neurotoxic Phormidium formosum Delayed effect Trichodesmium lacustre other

13 Toxic cyanobacteria in Norwegian lakes Woronichinia Planktothrix Microcystis

14 Algal toxins Type 2. Toxins that accumulate in mussels, fish, birds and mammals, and are toxic to humans (or mouse) Based on symptoms 1. PSP=Paralytic shellfish poisoning 2. DSP=Diarrheic shellfish poisoning 3. ASP=Amnesic shellfish poisoning 4. NSP=Neurotoxic shellfish poisoning 5. CFP=Ciguatera fish poisoning 6. AZP=Azaspiracid poisoning Based on chemistry 1. Saxitoxin group (PSP) 2. Okadaic acid group (DSP) 3. Pectenotoxin group (DSP) 4. Domoic acid group (ASP) 5. Brevetoxin group (NSP) 6. Yessotoxin group 7. Azaspiracid group (AZP) 8. Cyclic imine group

15 PSP - Paralytic shellfish poisoning toxins and algae (more than 20 different tetrahydropurins) Alexandrium tamarense

16 PSP - Paralytic shellfish poisoning Acute symptoms: Diarrhoea, nausea, vomiting, tingling sensation, respiratory and muscular paralysis (lammelser) Incubation time: 5-30 min Duration: Days Poisoning: About 2500 reported cases before 1993, 1-14% death rate. Some lighter cases in Norge, no death.

17 PSP - Paralytic shellfish poisoning other algae dinoflagellates Pyrodinium bahamense Gymnodinium catenatum Cyanobacteria: Anabaena spp.

18 Occurrence of PSP Increase in geographic distribution and frequency Cases since 1972

19 DSP - Diarrhetic shellfish poisoning Dinophysis spp. toxins and algae D. acuta D. norvegica D. acuminata D. rotundata Prorocentrum lima Okadaic acid (OA, okadasyre), dinophysis toxins (DTX), and pectenotoxins (PTX) are polyethers.

20 DSP -Diarrheic shellfish poisoning Symptoms: Gastrointestinal symptoms (diarrhoea, nausea, vomiting, abdominal pain), headache. Tumour promotion? Incubation: 30 min-12h Duration: a few days Poisoning: Many thousands of cases in Europe, Asia and Australia/New Zealand. Similar symptoms to bacterial infection. No death.

21 DSP occurence First time reported from Japan in 1976 Responsible algae: Dinophysis spp. Prorocentrum spp.

22 CFP - Ciguatera fish poisoning Toxins and algae maitotoxin polyethers

23 CFP - Ciguatera fish poisoning Related to consumption of tropical and subtropical marine fish (e.g. barracuda, red snapper, grouper) from some coral reef areas Symptoms: gastrointestinal symptoms, neurotoxic, reversal of hot and cold sensation Poisoning: More than persons are estimated to be poisoned every vear % death rate. It may take months or years to recover.

24 CFP occurrence Tropical distribution, especially in the French Polynesia

25 ASP-Amnesic shellfish poisoning Toxin and algae Pseudo-nitzschia spp., diatom (kiselalge) Domoic acid (DA, dominsyre)

26 ASP - Amnesic shellfish poisoning Symptoms: Gastrointestinal symptoms (diarrhoea, nausea, vomiting, abdominal cramps), headache. Desorientation. Amnesia (hukommelsestap). Neurotoxic Poisonings: First recorded in Canada in 1987 when 105 persons were poisoned and 3 died. Death rate 3%. No cases in Norway.

27 ASP occurrence Mainly in USA and Canada. Also detected in NZ, Ireland, Spain and Denmark (a few times in Norway)

28 New toxins in marine dinoflagellats Spirolides/ cyclic imines in Alexandrium ostenfeldii (unknown effects in humans) Yessotoxins in Protoceratium reticulatum (unknown effects in humans) Azaspiracids in Azadinium spinosum (similar to DSP)

29 Azaspiracid poisoning (AZP) Azadinium spinosum produces azaspirasids (AZA) that may cause illnesses in humans upon consumption of shellfish. Symptoms are similar to DSP. Azadinium spinosum is a small dinoflagellate Tillmann et al. 2009

30 Cyanotoxins Hepatotoxins: -microcystins (cyclic heptapeptide) -nodularin (cyclic heptapeptide) -cylindrospermopsin (alkaloid) Neurotoxins: -saxitoxin (alkaloid) -anatoxin-a (alkaloid) -homoanatoxin (alkaloid) -anatoxin-a(s) (ester) Skin irritants: -Lipopolysaccarids (LPS) -Lyngbyatoxin-a

31 Chemical structure to cyanotoxins polypeptides alkaloids alkaloid ester

32 Type 3. Ichthyotoxic (= toxic to fish) Toxic algae that harm or kill fish and other aquatic organisms, but are not toxic to humans

33 Ichthyotoxic blooms in Norway Karenia mikimotoi 1966, amost every year Chrysochromulina polylepis 1988, 1989, 1994, 1995 Chrysochromulina leadbeateri 1991 Prymnesium parvum yearly Pseudochattonella farcimen (=Verrucophora farcimen ) 1998, 2000, 2001

34 Ichthyotoxic haptophytes (svepeflagellater) Prymnesium Chrysochromulina Phaeocystis pouchetii

35 Chrysochromulina polylepis bloom 1988 Illustrasjon: Einar Dahl

36 Effects of the Chrysochromulina polylepis bloom in May-June 1988

37 Chrysochromulina polylepis bloom in 1988: effects on zooplankton

38 Long time-series of Chrysochromulina spp. in Skagerrak Chrysochromulina spp. Cells*106 l PO Year NO NO2 2.0 NH4 8 SiO4 25 Tot N Tot P 0.25 Part.P 80 (NO2+NO3):PO NO3:PO Tot N: Tot P NO3:SiO Chla:NO Chla:SiO Chla:PO4 Lekve et al year

39 Distribution of Prymnesium parvum observed bloom

40 Habitat: Prymnesium blooms low salinity (0,8-12 PSU) Limited area (pond, lake, fjord, lagune, river) nutrient rich Moderate to high water temperature Fish kills usually only at high algal concentrations (> cells L -1 )

41 Prymnesium toxins - structure A. hemolysin (Kozakai et al. 1982) B B. prymnesin-2 and N-acetylprymnesin-2 (Igarashi et al. 1996)

42 Prymnesium in Ryfylke, 1989

43 After 1995 Fishfarms disappeared from the area Prymnesium was rarely observed and when, at very low concentrations New fishfarms (Erfjord Stamfisk) were established in 2005 in Hylsfjorden (cradle of the booms) 2007 a toxic bloom of Prymnesium parvum killed 135 tons of caged fish From Eikrem et al. 2009

44 From Eikrem et al A submergible fish net was mounted over the fish enclosures during the toxic outbreak preventing the fish from entering the toxic brackish layer. The fish lost weight, but no mortalities was observed.

45 Bloom of Pseudochattonella farcimen in March 2001 mu From: Nansen Senter / CCMS-PML / NASA seawifs project 10 µm satellite image showing chlorophyll a concentrations

46 Are harmful blooms increasing in frequency? Possible explanations 1. Increased awareness and knowledge 2. Increased aquaculture activities and use of marine resources 3. Increased anthropogenic exposure 4. Increased transportation and dispersal

47 Some useful links to HAB web pages

48 Algal monitoring Started in stations Weekly cell counts of harmful species Reports on the web (algeinfo) Run by IMR, NIVA, SINTEFF, FD

49 Summary Most algal blooms are non-toxic. Phytoplankton are important as primary producers in the food web In the sea ca 2% of the microalgae may be harmful, most are flagellates. In freshwater mainly cyanobacteria are toxic Some toxins accumulate in clams and other animals. Others kill aquatic organisms directly. Harmful algae cause health, environmental and economical problems. Reported HABs have increased in distribution, frequency and intensity Increased problems are probably caused by increased awareness and antropogentic activity