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 4400/4320 2009 Bente Edvardsen 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 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 Noctiluca scintillans Luminescence (morild) heterotrophic dinoflagellate Not all red tides are harmful Blooms of cyanobacteria in fresh water Akersvannet, Vestfold Kolbotnvannet 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 Harmful effects • Toxic mussels and fish • 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 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 Economical losses for the aquaculture industry The ‘algal catastrophe’, Skagerrak, May 1988 Skagerrak 28 March 2001 Harmful algae in the sea In Norway Potentially toxic in Norway Algal class Nodularia spumigena BLÅGRØNNALGER (Cyanophyceae) FUREFLAGELLATER (Dinophyceae) SVEPEFLAGELLATER (Prymnesiophyceae) Alexandrium tamarense Alexandrium ostenfeldii Dinophysis acuminata Dinophysis acuta Dinophysis norvegica Karenia mikimotoi Protoceratium reticulatum Azadinium spinosum Chrysochromulina polylepis C. leadbeateri Prymnesium parvum Alexandrium minutum Prorocentrum minimum Prorocentrum lima Chrysochromulina spp. Pseudo-nitzschia multiseries P. seriata P. calliantha KISELALGER (Bacillariophyceae) NÅLFLAGELLATER (Raphidophyceae) Heterosigma akashiwo Olistodiscus lutheus KISELFLAGELLATER (Dictyochophyceae) Pseudochattonella farcimen Dictyocha speculum About 2% (ca 100 of 5000) of the marine microalgae are potentially toxic or harmful Harmful algae in the sea Haptophytes (Svepeflagellater ) Photo Karl Tangen Photo Wenche Eikrem Prymnesium Protoceratium Chrysochromulina Alexandrium Dinoflagellates, fureflagellater Photo Lars Naustvoll Pseudochattonella Silicoflagellates (kiselflagellater) Karenia Dinophysis Toxigenic cyanobacteria in Norwegain lakes Order Species Chroococcales Microcystis aeruginosa Microcystis botrys Snowella lacustris Woronichinia naegeliana Anabaena lemmermannii Anabaena flos-aquae Anabaena circinalis Anabaena solitaria Anabaena planctonica Anabaena crassa Anabaena tenericaulis Aphanizomenon flos-aquae Planktothrix agardhii Planktothrix rubescens Phormidium formosum Trichodesmium lacustre Nostocales Oscillatoriales Toxin Type of poisoning Polypeptides Hepatotoxic Delayed effect other Polypeptides Hepatotoksisk Alkaloides Neurotoxic Unknown Delayed effect other Polypeptider Alkaloider Hepatotoksisk Neurotoxic Delayed effect other Toxic cyanobacteria in Norwegian lakes Woronichinia Planktothrix Microcystis Algal toxins Type 2. Toxins that accumulate in mussels, fish, birds and mammals, and are toxic to humans (or mouse) Based on symptoms 1. 2. 3. 4. 5. 6. PSP=Paralytic shellfish poisoning DSP=Diarrheic shellfish poisoning ASP=Amnesic shellfish poisoning NSP=Neurotoxic shellfish poisoning CFP=Ciguatera fish poisoning AZP=Azaspiracid poisoning Based on chemistry 1. 2. 3. 4. 5. 6. 7. 8. Saxitoxin group (PSP) Okadaic acid group (DSP) Pectenotoxin group (DSP) Domoic acid group (ASP) Brevetoxin group (NSP) Yessotoxin group Azaspiracid group (AZP) Cyclic imine group PSP - Paralytic shellfish poisoning toxins and algae (more than 20 different tetrahydropurins) Alexandrium tamarense 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. PSP - Paralytic shellfish poisoning other algae dinoflagellates Pyrodinium bahamense Gymnodinium catenatum Cyanobacteria: Anabaena spp. Occurrence of PSP Increase in geographic distribution and frequency Cases since 1972 DSP - Diarrhetic shellfish poisoning toxins and algae Dinophysis spp. D. acuta D. norvegica D. acuminata D. rotundata Prorocentrum lima Okadaic acid (OA, okadasyre), dinophysis toxins (DTX), and pectenotoxins (PTX) are polyethers. 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. DSP occurence First time reported from Japan in 1976 Responsible algae: Dinophysis spp. Prorocentrum spp. CFP - Ciguatera fish poisoning Toxins and algae maitotoxin polyethers 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 50 000 persons are estimated to be poisoned every vear. 0.1-12% death rate. It may take months or years to recover. CFP occurrence Tropical distribution, especially in the French Polynesia ASP-Amnesic shellfish poisoning Toxin and algae Pseudo-nitzschia spp., diatom (kiselalge) Domoic acid (DA, dominsyre) 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. ASP occurrence Mainly in USA and Canada. Also detected in NZ, Ireland, Spain and Denmark (a few times in Norway) 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) 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 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 Chemical structure to cyanotoxins polypeptides alkaloids ester alkaloid Type 3. Ichthyotoxic (= toxic to fish) Toxic algae that harm or kill fish and other aquatic organisms, but are not toxic to humans Ichthyotoxic blooms in Norway Karenia mikimotoi 1966, 1974-1991 amost every year Chrysochromulina polylepis 1988, 1989, 1994, 1995 Chrysochromulina leadbeateri 1991 Prymnesium parvum yearly 1989-1995 Pseudochattonella farcimen (=Verrucophora farcimen ) 1998, 2000, 2001 Ichthyotoxic haptophytes (svepeflagellater) Prymnesium Chrysochromulina Phaeocystis pouchetii Chrysochromulina polylepis bloom 1988 Illustrasjon: Einar Dahl Effects of the Chrysochromulina polylepis bloom in May-June 1988 Chrysochromulina polylepis bloom in 1988: effects on zooplankton Long time-series of Chrysochromulina spp. in Skagerrak 0.6 0.4 0.0 0.2 Cells*106 l-1 0.8 1.0 Chrysochromulina spp. 1990 1992 1994 1996 Year PO 4 0.6 1998 NO 3 10 2002 NO 2 0.6 5 0.2 0.0 0 2.0 2000 NH 4 SiO 4 4 0.5 Tot N 25 8 15 0 Tot P Part.P 1.0 0.25 0.4 0.05 (NO 2 +NO 3 ):PO 4 80 40 0 NO 3 :PO 4 80 60 Chla:NO 3 40 20 20 10 0 0 1992 1994 1996 1998 2000 2002 NO 3 :SiO 4 2 20 0 6 4 40 40 Lekve et al. 2006 Tot N : T ot P 0 Chla:SiO 4 150 Chla:PO 4 50 0 1992 1994 1996 1998 2000 2002 year 1992 1994 1996 1998 2000 2002 Distribution of Prymnesium parvum observed bloom Prymnesium blooms z Habitat: – low salinity (0,8 - 12 PSU) – Limited area (pond, lake, fjord, lagune, river) – nutrient rich z Moderate to high water temperature z Fish kills usually only at high algal concentrations (>100.106 cells L-1) Prymnesium toxins - structure A. hemolysin (Kozakai et al. 1982) B B. prymnesin-2 and N-acetylprymnesin-2 (Igarashi et al. 1996) Prymnesium in Ryfylke, 1989 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 From Eikrem et al. 2009 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. Bloom of Pseudochattonella farcimen in March 2001 mu 10 µm satellite image showing chlorophyll a concentrations From: Nansen Senter / CCMS-PML / NASA seaWiFS project 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 Some useful links to HAB web pages • http://www.whoi.edu/redtide/index.html • http://www.issha.org/ • http://ioc.unesco.org/hab/news.htm • http://algeinfo.imr.no/ Algal monitoring • Started in 1989 • 56 stations • Weekly cell counts of harmful species • Reports on the web (algeinfo) • Run by IMR, NIVA, SINTEFF, FD 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