Toxic and harmful marine phytoplankton and microalgae (HABs) in Mexican Coasts

Toxic and harmful marine phytoplankton and microalgae (HABs) in Mexican Coasts

DAVID U. HERNANDEZ-BECERRIL', ROSALBA ALONSO-RODR~GUEZ', CYNTHIA ALVAREZ-GONGORA'. SOFIA A. BARON-CAMPIS*. GERARD0 CEBALLOS-CORONA5. JORGE HERRERA-SILVEIRA3, M A R ~ A E. MEAVE DEL CASTILL06, NORMA JUAREZ-RU~Z~, FANNY MERINO-VIRGILIO', ALEJANDRO MORALES-BLAKE7, JOSE L. OCHOA8, ELIZABETH ORELLANA-CEPEDA9, CASIMIRO RAM~REZ-CAM ARENA^ and RACIEL RODR~GUEZ- SALVADOR^^ 'Lrrl~luto de Ciencias del Mar y Lhnologia, Urtiver.ridad Nacional Aurdnoma de Mixrco ( U N A M ) . MGxico, D.F. , Me.uco 'Lrrliruro de Cie~lcias del Mar y Lhnologia, Cambior Unidud Acadhnica Mazorldn onres de Insriruro dc Ciencia del Mary L~mologia , Mazarlan. Sinaloa, Mcxico

Cenrra de Invesrigociones y Esrudios Avanrados, Unidnd Mirida, Mirida, Yucartin, Me.vico 41nrri~ulo Nacu~nol de la Pesca, SAGARPA, Mi.~ico, D F , Me.~ico 5Fac. Biologia, Universidad Micl~oacana dc S w Nicol6s de Hidalgo. Morelin. Micl~onch~, Mexico 6Dcp~o. Hi&obiologia. Univrrsiiad Auronoma Mcrropolitmm Izrapalapa, ME.rico, D . K , Mrxico 7Faculrad de Ciencios Morinac. Unzvemidod de C o l h a , Manranillo, Col"m, Mexico SCerrrro dP lnvesrigociones Biolbgicos del Noroesre, L a Paz, B.C.S., Mexico 9 F a ~ ~ l r u d de Cien~ios Morinm, Universidad Aur6noma de Baja Califurnik, Emenadu. B. C.. M6xico ' "C E T M A R , Ptrrrro Madero, Chiopas. Mexico

Harmful Algal Blooms (HABs) are becoming an increasing prohlem to human health and environment (including effects on natural and cultured resources. tourism and ecosystems) all over the world. In Mexico a number of human fatalities and important economic losses have occurred in the last 30 years because of these ewnts.Thereareabou 70swiesofplanktonicand non-planktonicmicroal.~e considered harmful in Mexican foasts. The most important toxin-producing species are the dinoflagellates ~ ~ k o d i n i w n corrna& and Pvrodlniwn bahameme var. coworessum. in the Mexican Pacific. and Karenio brevis in the Gulf of Mexico. and conxauentlv the ponso&s documented in Mexico are ~aral;tic Shellfish Poisoning (PSP) and Neurotoxic Shellfish Poisoning (NSP). ~ l t h b u ~ h ;here is evidence that Amnesic Shellfish Poisoning (ASP), Diarrhetic Shellfish Poisoning (DSP) and Ciguatera Fish Poisoning (CFP) also occur in Mexico, these problems are reported less frequently. The type of phytoplankton and epiphytic microalgae. their toxins and harmful eKects as well as current me tho do lo^ used to study these phenomena are presented in this paper. As an experienced group of workers, we iuclude description~s of mouitoril~g and mitigatiou programs, our proposals for collaborative projects and perspectives on future research.

Keywords: Biotoxins; harmful algal blooms; marine phytoplankton; Mexican coasts; microalgae.

Introduction

Mex~co IS a large country that has coasts In two Oceans the Paclfic and the Atlant~c Thus, there are many drf- ferent env~ronmental cond~t~ons (golog~cal, cl~matologs and oceanogaphs ones) and drverse habrtats and envl-

Address correspondence to David U. Hernandez-krril. Insti- tuto de Ciencias del Mary Limnologa, UNAM, Aplo. postal 70-305. Mtxico. D.F.. Mexico; E-mail: [email protected]. unam.mx

cons (oceanic zones, coastal areas with extensive or re- duced shelves, coastal lagoons, deltas of various rivers, is- lands, coral reefs, mangroves) where diverse marine flora and fauna develop. These natural resources are very important, but have been subject of ongoing threat and de- terioration. Recent increase of cases of toxic and harmful marine phytoplankton and microalgae is an issue that must be assessed to understand the consequent impact to human health, fisheries and tourism.

World research on toxic and harmful marine phytoplankton and microalgae has consequently augmented and various scientific organizations and international

1350 Hernrindez-Becerr et al.

programs (e.g., Harmful Algal Bloom-HAEpmgram, from the International Oceanographic Commission-1OC-, of UNESCO, and subsequently ECOHAB, GEOHAB and EUROHAB) have been created to address correspon- dent investigations on the topic, trying to cover all possible disciplines During more than 30 years the world has observed species arising as toxic and harmful, causing disturbances and noxious effects 011 marine life and humans, new concepts and hypothesis proposed to explain the expansion and increase of HABS?.)]

"Red tides" are regarded as bio-optical phenomena and "rely implicity on a threshold of plant biomass or light extinction." whereas blooms are rather ecophysiological phenomena "typically harmless" ("originally the regular spring growth in temperate and where biomass and populations density are important issues.[5] The term Harmful Algal Blooms (HAB) has become of common use among scientists and refers not only to phytoplankton, but also to non-planktonic algae.

The importance and diversity of the marine phytoplankton, microalgae that shift freely in the pelagic realm and which are mostly photosynthetic. has been already em- phasized in Mexico,16.'1 and other previous papers also dealt with the toxic and harmful marine phytoplankton, the phytoplankton that can produce toxins that affect marine life and also humans or can cause harmful cases due to high den~ities;[~-l~l other non-planktonic marine microalgae (e.g., tychoplanktonic, benthic, epiphytes) have been less treated and often are considered part of the phytoplat~kton!~~]

Marine phytoplankton and epibenthic marine microalgae

Marine phytoplankton is an ambiguous term, which de- fines a community of microalgae, mostly photosynthetic, inhabiting the pelagic marine realm.['] The important eco- logical roles of the phytoplankton in the sea are as primary producers, linking inorganic sources of energy into upper trophic levels, and participating in fundamental cycles of some elements in n a t ~ r e . l ~ ~ ~ ' ~ ]

The number of species within this community is nearly 5000 extant species:["l between 3444 and 4375 species,["' with 15 to 20 taxonomic classes (most classes of algae are represented in the plankton). In Mexico, an esti- mate of the number of marine phytoplankton taxa yielded approximately 1488, within 21 1 genera; this figure represents only the 33 to 42% of the total number proposed for the whole world.171 The most studied groups are diatoms (Bacillariophyceae) and thecate dinoflagl- lates (Dinophyceae), which largely contribute to the diversity and very often also to biomass in the marine phytoplankton. Two other groups less studied are silicoflag- ellates (Dictyochophyceae) and coccolithophorids (Hapto- phyceae); these 4 groups are "preservable" forms, which are usually collected and studied with no special proto-

col. The rest of the taxouomic groups are the so-called "phytoflagellates" (planktonic and photosynthetic flagellates) and cyanophytes (Cyanophyceae. Cyanobacteria), unique group of Procaryotes in the phytoplankton. From this large diversity, the species reported as forming "red tides" are 184-267 (about 300 species), whereas the species considered producing toxins are 6&78, from which the ma- jority are dinoflagellates (73-75%).[1.'.4.191

Species of various goups produce toxins or are harmful to marine organisms and human health. Some species can be nuisance in some circumstances: dense populations may lead to high consumption of oxygen and liberation of toxic substances (eg., hydrogen sulphide) that can kill fish, or interfere with the digestion of flagellates by shellfi~h.[~"1 In Mexico, there are about 70 species of microalgae belouging to six taxonomic groups considered harmful in the littorals of the Atlantic and Pacific Ocean. OF them, the most diverse are the dinoflagellates: 47 taxa (46 species and one variety), diatoms (I 5 species), Raphidophytes ( 6 5 species), and 3 species of Cyanobacteria. I Haptophyte and 1 Dic- tyochophyceae (Table 1).

The dinoflagellates Gynvrodiniunr carenarunr and Pyro- dinium bahamense var. compressum, in the Mexican Pacific, ar~d Karenia brevir in the Gulf of Mexico (Figs. 1, 2), are known for their toxicity. Other dinoflagellates considered to be toxin producing (either to humans and marine fauna) and that have been found in Mexican waters, with prelimi- nary or no documentation of having produced any toxic event in Mexico, are: Akadriwo sunguinea, Alexandriwn acarenella, A. carenella, A. leei, A. minurwn, A. monila- irm, A. osrenfeldii, A. ranrarense, A. ramiyavaniclrii, Coclrlo- dinium polykrikoides, Dinophysir acwninara, D. caudara, D. forrii, D. n~irra, D. rorurtdota, D. rripos, Ganrbierdir- cur roxicus, Linguladntium polyedra, Ostreopsis 1enriculari.s. 0.sianrensir. Proroccnrru~n concavwn, P. rntarginalunr, P. linra. P. nrexrcatunl. P. nzutinrunt, P. rharhyntum. Proro- cerariwn rrricularwn, Proroprridiniwn crassiprs and Pyro- diniwr bahatneme var. balranwnse (Table 1, Figs. 1,2). From this list, only Gambierdiscus toxicus. Osrreopsis species and most probably Prorocenrrunr luna are non-planktonic forms.[21-2'1

Gynu~odiniunl carowrunr is the only gymnodinoid dinoflagellate that produces saxitox~ns and related toxins causing Paralytic Shellfish Poisoning (PSP). This is an athecate (naked), photosynthetic, chain- and cyst-forming dinoflagellate that hasincreased itsglobal distributionall over the world (in temperate to subtropical areas). Originally described from the Gulf of ~alifornia,[~'1G. carenarum is an important component of the phytoplankton along the Mexican Pacific coasts, from the Gulf of Calif0rnia['~-"1 (Fig. 1, 2).

The thecate dinoflagellate Pyrodiniunr bahanteme var. con~pressun~ is considered a variety of the type species, P. balmreme, the latter shows no evidence of toxicity, until very re~entl~.l'~1 It has a number of tiny plates in the theca, cingulum and sulcus, and differs from the type variety for

Pliytoplankton and H A 6 microalgae in Mexican Coasts

Table 1 . HABs species in coasts of Mexico

Carrrarive species

Dinoflagellates Alcxandrium acarcnclla (Whedon er Kofoid) Balech Alr.vandrium carrnclla (Whedon cr Kofoid) Balech Alexandrium leei Balech Alesandrium minurum Halim Alexandrium ntonilarum (Howell) Balech Ale.vandritun osrenfeldii (Paulsen) Balech el Tangen

Alesmdriwn ramorenye (Lehour) Balech Alexundrium rruttiynvunichii Balech G~mnodinilun carenaton Graham Pyrodiniwr bahamenre Plate var. Baltamense Pyrodiniwr bahammrrr var. conrprcv,vwn (Bohm)

Steidinger, Tester er Taylor Dinopl~ysir acuminara Clapasde er Lachmann Dbroplrysi caudara Saville-Kent Ditroplry.ri.vf&tii Pavillard Dinophysip miira (Schutt) Abi- DinopI~y.~ir rorundara ClaparMe el Lachmann Dirropltysip rripos Gourret Proroccnrrrun concal~um Fukuyo Prorocenrrtun emcrginnrwn Fukuyo Prorocenrrum limo (Ehrenberg) Dodge Prorocenrrum ntexrcanum OsonuTafa11 Prorocmrrum rhagstum Loeblich. Sherley rr

Schmidt

Illness -

PSP PSP PSP PSP PSP PSP

PSP PSP PSP PSP PSP

Carrrative species

Dinoflagellates Gambicrdircrrr roxicus Adachi cr Fukuyo Osrrcopsip lcmicularip Fukuyo Osrreopsip siatnensip Schmidt Karcnia brew (Davis) Hallsen et Moestmp Lingulodiniwnpvl.vcdra (Stein) Dodge Prorocerarllun rcricuhrwn (Claparede er

Lachmann) Biitschli Proroperiduriwn crarsipa (Kofoid) Balech

Diatoms P.reudo-nirz.vdria awtralip Frenguelli P.~cud~nir~.rcl~ia dclicariP.rum (Cleve) Heiden

DSP Pseudo-nitrsdlw fraurlulerlra (Cleve) Hasle DSP Pseudc-nitisd~io mulliverics (Hasle) Hasle DSP Pscrrdu-nirzsclria p.veudodclocarir.vin~a (Hasle) Hasle DSP Prcu&ntr:schin &,qms (Grunow 8.t Clevc) Hdsle DSP P,vrah,nrr:rdua suhl>audulrnra I Haslc) Haslc . . DSP DSP Cyanobacteria DSP Anahaena spp. DSP Microc.vsrip neruginosa Kiitz DSP Tricltodesmium rryrlwaewn (Ehreuberg) Gomont DSP Tr12hodmniwrr rhi?baurii Gomont PA. Gomont

Illness -

CFP CFP CFP NSP YTX YTX

A Z A

ASP ASP

ASP ASP ASP ASP ASP

CTP M C M C MC

'Illness or toxins: Paralytic Shellfish Poisoning (PSP), Amnesx Shelliish Po~wning (ASP). Ctpuatera. Fish Poionmg (CFP), Neurotoxic Shellfish Poisoning INSP), Cyanohacterial Toxin Poisoning (CTP), Yessoloxin (YTX), Micmcyslin (MC). Amsplraeids ( M A ) .

Gulf of

I Tehuantepec 1 Fig. 1. Map showiug Mexicau States with littorals and general distribution of some harmful s p i e s . I: Baja California, 2: Baja California Sur. 3. Sonora, 4: Sinaloa, 5: Nayarit, 6: lalisco, 7: Colima, 8: Michoacin, 9: Guerrero, 10: Oaxaca, II: Chiapas, 12: Tamaulipas, 13: Veracruz. 14: Tabasco, 15: Campeche, 16: Yucatan, 17: Quintana Roo. Gray circles: Gytnnodiniwn caretwtum, black circles: Pyrodutium bahamrrr~e var. compresswt. white circles: Lingulodiniwn polyedru. whlte squares: Alexandrium catenella black squares: Karenw breviF. asterisk Coclrlodiniwn polykrikoide,r.

1352 Hentartder-Becerril et al.

Fig. 2. Harmful species found in Mexican coasts (LM, except i. TEM). Dinoflarellates: a . Karcnia brcvD, b. Gvmnodbliwn carcnarwn, c . ~ y r o d k i w n bahamerue var. compressurn, d. ~ochloduriwn j&ykrrikoides, e. ~&ulodkiwn polyedra, t ~rof&ridkium crmipes, g. Ale.~andrrwn carenella. h. Dmoohvsu caudoro. Raohidoohvte: i. Cluronella m a r k . Diatom: i. k. Psedo-n~uschin ouneeny. a valve in . . . . . detail (TEM) and part of a ch%

Pliytoplankton and HAB microalgae in Mexican C o a t s 1353

being slightly depressed apical-antapicaly and usually forming short to long chains. P ba lmerne vat. cornpressm is now considered the most dangerous species in tropical regions because of its high toxicity and responsibility of 97% of human deaths by Paralytic Shellfish Poisoning (PSP). Hallegraeff and MacLean12'] estimated that toxic Py- rodiniuni has been responsible for more than 1,000 human illnesses and 60 fatalities resulting from the consumption of contaminated shellfish as well as planktivorous fish such as sardines and anchovies; Rosales-Loessenefi3"I pointed out that in coasts of Guatemala, 187 people were affected and 26 resulted in death in July, 1987, whereas in Costa Rica, 70 people were poisoned (December. 1999 to January. 2002).["1

The athecate dinoflagellate Karenia brevis, originally described as Gynsiodiniunr breve Davis, later named Pry- chodiscus brevis (Davis) Steidinger, and more recently pm- posed as a species of the genus Karen i~ , [~~] is a relatively small, ventraldorsal flattened and photosynthetic form, with no known resting stages, which produces hrevetox- ins (or neurotoxins) associated to the Neurotoxic Shell- fish Poisoning (NSP). The species is currently considered an endemic micmalga from the Gulf of Mexico: it is distributed from Texas, Alabama, Luisiana and Florida (USA) to the Peninsula of Yucatan (Mexico) (Figs. I, 2). Effects on the marine fauna because of neurotoxins in New Zealand were reported, although the responsible

8 species are differer~t/'-~~-'~l and the brevetoxins varied in s ~ N c ~ u R . [ ~ ~

Among diatoms, in Mexico we can consider the following potentially toxic, planktonic forms: Pseudo-nirzschia awrralis, P . delicariwinla, P. fraudulenra, P. rntclriseries, P. pseudodelicarissirna, P . pungens and P. subfraud~lenra~~~~"~ (Table I, Figs. 1,2). Surveys on "phytoflagellates" and phytoplankton studies in Mexican coasts revealed the wide occurrence of the Raphidophytes: Charonella marina, Ch. subsalsa, Fibrocapsa japonica and Hererosignta a k a r k i ~ o ! ~ ~ ] all of them considered to be toxic to fishes (Table 1, Figs 1, 2), and with very recent reports of toxic events. Other "phytoflapllates" have been also detected in Mexican waters (Table I), most of them innocuous, at the moment. Cyanobacteria potentially toxic that have been identified in Mexico are: Anabae~a sp., Trichodesntiunt erjirhraeunt and T . rhieb~urid'~l (Table I). Finally, it is important to include , those considered non-toxic or innocuous "red tldesV- forming species that are common in Mexico, and often cause alarm. The main causing species are the ciliate Miry-

man health, (ii) Natural and cultured marine resources, (iii) Tourism and recreational activities, and (iv) Marine ecosystem.[2] The following is a classification based on chemical characters:

Azaspiracidr ( A Z A ) . This is a new group of toxins which name derives with the ring Azaspir and the presence of a functional carboxyl. These are stable in solvents such as chloroform, under slightly alkaline conditions. They are produced by the thecate dinoflagellate Proroperidiniuni crassipes.

Breverosins (BTX) . Brevetoxinsare neurotoxic substances originally found in "red tides" and cultures of Karenia brevis. They are "ladder-shaped polycyclic ether compounds", with two types, A (defined as PbTx-1, -7, and -10) and B (defined as PbTx-2, PbTx-2 oxyded, -3, -5 -6, -8, and -9). Cells of K . brevis may break and release their toxins to the water, causingfish mortality in highconcentrations, and aerosols are carried to the coasts producing human irritations. Additionally, Neurotoxic Shellfish Poisoning (NSP) may be produced when oysters or other marine products contaminated by brevetoxins are consumed by human~.[~1 In Mexico, the maximum permissible level of BTX is 20 MU 100 g-I of shellfish tissue.[41]

Okadaic acid (OA) . Okadaic acid and its analogues, Dino- physitoxins (DTX I and DTXZ), are the main toxins responsible for the Diarrhetic Shellfish Poisoning (DSP). These are produced by species of the dinoflagellates Dutopliysis and Prorocenrrum. Shellfish containing more than 2 ~g OA and/or 1.8 gg DTXl per gram of hepatopancreas are not considered fit for human consumption.['] No documented cases in humans are recorded in Mexico so far.

Pecrenoroxins (PTX) . The name of these toxins comes from the genus of Scalops (Pecruiopecretr and Enssoensis), from which they were first isolated, and are also polycyclic ethercompounds. The toxinsareatrihuible to the thecate dinoflagellate Prorocerarim rericularurn. The toxin homoye- sotoxins (homo-YTX) is produced by another dinoflagellate. Lingulodiniurnpolyedra. Stability of these toxins is not well known as yet.

onecra rubra, some dinoflagellat& of the genus Cerariunr, Gonyaulax, Nocriluca scintillans, and various diatoms (Ta- Hyhophi'ic

hle I). Dontoic acid (DA) . Toxins causing ASP or Domoic Acid were originally isolated from the red macroalga Chondria armara, in Japan. After the incident in 1987 in Canada,

Toxins when over 100 people were sickened and 3 died,I4l] this toxin was identified as the causative in poisonings for shell-

There are numerous toxins produced by planktonic and fish consumption with very high levels Shellfish containing non-planktonic microalgae. They may be divided into four more than 20 ~g DA per gram of shellfish meat are consid- different categories, depending on their effects: (i) Hu- ered unfit for human c~nsum~tion!~] At the moment, there

are 9 to 10 Pseudo-nirrschia species known to produce the toxin domoic acid.I4']

Hermirdez-Becerril et al.

Results and observations

Saxiroxiru ( S T X ) . PSP is produced by a group of po- tent toxins termed saxitoxins, which include 2 dozens of different types. Toxins are produced by the dinoflagellates Gymnodinium carenaturn, Pyrodinium hahameme var. compressum and species of the genus Alexandriunt, although more recently they are also associated to the Cyanoba- terium Trirfrodcsniiunr cryrhracun~. This is one of the most common and dangerous poisoning around the world, that has caused numerous human fatalities, and some of the causative species have dispersed wider in the world (as G. carerrarum and P hahamense var. ~om~ressum)!~' l

Garate-Lizirraga et al.[441 provided PST's profiles on different strains of G~'mnodinium corenorum from three bays in the Gulf of California. The toxin profile for the different strains of Mexico is: dcSTX, dgGTX2, GTX3, B1, B2 and C2 STX and neoSTX. Toxin content varied from 36.1 to 184 pg cell-'; the strain from Mazatlan was the most toxic. The toxic composition appears not to be a con- servative property in G. carorarum, however other studies havedemonstrated a consistency in the toxin profile within population. Toxin composition may vary among microal- gal species and strains with geographical locations, with environmental factors, and under different experimental conditions.[45]

Other toxins

Ciguatera is a circum-tropical syndrome well-known in the Caribbean. French Polynesia and Australia, which is currently associated to the high populations of benthic dinoflagellates, such as Ganzbierdircrcr roxinc~. 0srreopsi.s lenricularis, 0. siamensis and perhaps Prorocenrrum limo. The toxins related to this poisoning include Ciguatox- ins, Gambiertoxins and Maitotoxins, which accumulate through the food chain, from small fishes grazing on coral reefs or larger aquatic plants into muscle and organs of bigger fishes.

There are a number of other toxins which cause no effect on humans but in the marine fauna (mainly fish and shellfish), and eventually are nuisance to aquaculture, tourism and environment. Almost all marine Raphidophyte species are considered to be toxic to fish, by producing Reactive Oxygen Species (ROS) as superoxide anions, hydroxyl rad- icals, singlet oxygen, and hydrogen peroxide, which princi- pally affect fish as other organism^,[^^^ and other "phytoflagellates" produce other ichtyotoxins (Table I). The symptoms of fish are not specific of raphidophyte bloom, both physical clogging of fish gills by mucus excretion as well as gills damage by hemolytic substances may be in~olved."'-~~1 Free fatty acid production, notably of eicosapentaenoic acid may also play a role in fish mortalities caused by these blooms[49]

Eflects of KABs on hum^ health

Typical poisonings in coasts of Mexico include NSP and PSP, but there are also some other poisonings that have been less documented and they are gaining importance: ASP, DSP and minusc Ciguatera. As these intoxications put at risk human health, popular concern grows, and thus these are the best documented poisoning.

Karenia brevis and helveric NSP In coasts from the Gulf of Mexico, mass fish mortalities have been reported since pre-hispanic times and then frequently between 1797 and 1995.1"l Many cases have been documented in Texas, Louisiana and Florida, USA since 1844.1'01 However, it was until 1947 when dinoflagellate Karcnia brcvis was identified as the species respo~lsible for the production of neurotoxins (and NSP) and the causative of fish m0rtali t~.[~~1

In Mexican coastal waters there are only 2 official reports previous to 1995.[8.5'1 However, during the period 1 9 9 6 2005 several blooms of K. hrevis have occurred in Mexico, causing mass mortality of fish and other marineoganisms and general respiratory effects in humans in Tamaulipas, Veracruz and Tabasco. The economic impact of these losses was not properly evaluated (e.g., fisheries, tourism, health), althou* banning of fishing oysters was determined.

Data recorded during 9 yearsindicate that October is the month with higher cases of "red tides" caused by K. brevis (Table 2) and that blooms of the species originally coming from Texas. USA, might be transported by coastalcurrents to Mexican coasts, affecting Tamaulipas and Veracn~z.[~~] Different hydrographic and oceanographic processes do occur in the Gulf of Mexico, and a closely relation between physical processes and the blooms caused by Karenia brevis has been found.lS4]

Gyntnoduriunr cacenarunr and PSI! Human fatalities in Mexico are associated, in most of the cases (if not all), to the paralytic toxins, in the Mexican Pacific. The 2 causative species are identified as Gynu~odinium carenarwn and Pyro- dinium bahamense var. corrrpressuni, although their distri hu- tion apparently does not overlap: G. caremrum distributes from the upper GuIfof California to Acapulco, Guerrero, whereas P. bahan~ense var. conlpressunr has a distribution from Costa Rica to Manzanillo, Colima, thus both species share a transition zone, but do not appear to occur at the same time["] Alexartdriunt carenella is the causative dinoflagellate for PSP in western coast of Baja Cahfornia; this species is a regular phytoplankton member, but rarely it is observed in high densities (2.5 x LO4 cells L-' in summer), nevertheless, these lower cell concentrations are capa- ble of generating very high level of PSP toxins in shellfish, although there is no documented evidence of human poisonings.

Pl~yloplanklon and HAB microalgae 1n Mexrcan Coasts 1355

Table 2. lnformat~on on HABs caused by Kurmm brcwrr In coasts of Mex~co fmm the Gulf of Mex~co (199G2005)

Location Cell obundances Toriciry Dote (State) (cells L-I) (MU 100gr- ' ) Remarks

1996 October Tamaulipas - - Losses of 4.5 Tons fish. Respiratory irritations. 1997 October Tamaulipas 13-279 x 10 ' 1049.6 Losses of 80 Tons fish. Respiratory irritations. 1999 October Tamaulipas LC-260 x 10' 46 Short event 2000 October Tamaulipas 5 x 10' - Short event, fish mortality 2001 December Veracruz 3.S739 x 10' LC-207.2 Oyster beds closed fromOctober, 2001 to February; 2002. 2005 May-July Tabaxo 1404 143 x 10' 1C-306 Daily losses of 800 Kg fish. Respiratory irritations.

There have been 561 sickened and 38 dead people from 1970 to 2004, with a rate of mortality close to 6%. High concentrations of the species have been reported with few human fatalities, and also fish m ~ r t a l i t i e s . [ ' ~ ~ ~ ~ ~ The first documented case occurred in Mazatlan Bay in 1979, with several poisoned people[551; high densities of the species (up to 1.14 x lo6 cells L-l) and March and April as the species blooming period have been

Pyrodinium bahamense var. compressum and P S P In the southern Mexican Pacific, one of the first documented HAB produced by Pyrodinium hnhomense var. compres- sun1 occurred in November, 1989, in the Gulf of Tehuante- pec. It caused 99 poisoned people and 3 deceases by consumption of shellfish Osrreo iridiscens and Chmronryrilus polliopuncran~r.~571

More than 200 people have been affected and 6 have died for PSP due to saxitoxins produced by P. buhante~ue var. compressum. From November, 1995 to February, 1996, a bloom of the species reached coasts of Michoacan and Guerrero, causing 6 human fatalities and many more affected people by high toxicities were detected in Osrreo iridiscem (Table 3). From November, 2001 to August. 2002. HABs coming originally from Chiapas (patches of 1 357 km), reached coasts of Guerrero (Table 3). During 2001 HABs in Puerto Madero, Chiapas cysts of the taxon a p peared in the water column 3 months before (January) than vegetative cells did (March). In May cysts disappeared from the water column and again were found in August with a maximum density (60,000 cysts L-I), coinciding when the

vegetative cells reached their maximum densities (180,000 cells L-I). This was interpreted as a new generation of ~ ~ s t s . [ ~ ~ 1

In Mexico HABs by P hoho~r~ese var. compressunr have occurred withintervals of 3 to 5 years(winter 1989,Novem- her, 1992, November 1995 to February 1996, January 2001 to February 2002, and beginning of 2006) and always the first trace of the species started in coasts of Chiapas in the Gull' of Tehuantepec, a region characterized by occurrence of winter upwellings. These HABs may be associated with those upwellings, but insome occasions this taxon is present in the water column by several months and the highest densities have been observed seven months after upwellings, during the rainy season ( A ~ g u s t ) ! ~ ~ ~

Other poisonings

Cipatera is a syndrome known mainly in the Mexican Caribbean, but there are few reports that it also occursin the Mexican Pacific.P91 Some of the most important causative species have been found in the Mexican Caribbean, such as the dinoflagellates Gambierdi.mu roxicus, G. bekeanus and G. yasun~oroi.[221 The symptoms of this syndrome mask other illnesses and thus it is difficult to asses its real distribution and some other origins of toxins. In this area, it has been established that the most critical period for Ciguat- era is July and August, which led to ban certain fisheries; the main spot where reports have been made is Isla Mu- jeres In the last 5 years, 17 people have been reported to be poisoned, with no decision.

Table 3. Information on HABs caused by Pyrodinium bohamense var. compressrun (with PSP aflections) in the southern Mexican Pacific (1989-2006)

Dare

1989 November Gulf of Tehuantepec 1.7 x 106 81 1 99 poisolled persons, 3 death

1995-1996 (Nov-Feh) Michoacan and Guerrem - 6 337 6 death persons 2001-2002 (Nov-Aus) Chiapas to Guerrero 3.5 x 106 7 309 101 persons

poisoned. 6 death. 48 Tous fish killed

200S2006 (Dec-Mar) Puerto Madero, Chiapas 1.8 x loJ 200 -

Herndndez-Becerril et al.

Effects of HABs on the norural resources, envirommrnt and economy

No confident evaluation has been yet done on the economic loss due to HABs in Mexico, only in some cases this loss is calculated for the industry arected, therefore, there are not national statistics about losses caused by harmful algae events.

HABs r i~ the Gulfof Mexico

Apart from the Karenia brews reports in coasts of the Gulf of Mexico and Caribbean Sea. there is scarce documentation of HABs A recent account on toxic and harmful dinoflagellates from the southern Gulf of Mex- ico has been given by Licea et a1..[60] An innocuous "red tide" lasting 20 days appeared in the port of Veracruz, November, 2002, caused by the dinoflagellate Periditriunt quinquecort~e,[~~~

HABs in t k Northern Mexican P a 4 c

In western coasts of Baja California, Lingulodinium yo@ dra is one of the dominant dinoflagellates, which has been historically documented from 1902 off La Jolla, California. USA.16" The conceptual model of L. polyedra was postu- lated by Orellana-Cepeda et a1..[6'] and the cysts were studied in Todos Santos Bay sediments by Peha-Manjarrez et a1 .Y During blooms of L. polyedra, densities may be as high as 10' cells L-I, and there is a dissolved oxygen deficit, causing the mortality of sensitive species on the bottom. When density reaches 106 cells L-I. "marine snow" covers surface water and light cannot penetrate. causing ecologic disasters and fishes, crustacean, octopus and other benthic resources have died. By February, 1996. in Todos Santos Bay. Baja California. L. polyedra was the most abundant species (7.93 x 10' cells L-I). The dinoflagellates Proro- cenlrwr micanr and Akashiwo sanguitrea are also regularly recorded. mainly during HABs and these species can also generate small quantities of hydrogen peroxide. Another dinoflagellate. K m t i a mikimoroi, has a highest concentra- tion in upwelling areas during the autumn. The raphidophytes Fribocapsa japonica, Charonella anriqua, Ch. ntarina. Heterosigma akashiwo and the dinoflagellate Cochlodinium po1ykrikoide.r are the most important potential ichtyotoxic species in the area, which have maximum densities on September.

The planktonicdiatoms Pseudonirz~chiaausrrali.$, P: mul- rireries, P: delicariisbna, P subjraudubrra and P: pungetrr do occur in the area, with maxima values during spring and minima during the winter. Pseudo-nirzschia species have been associated with domoic acid production and poisonings of marine mammals. In 2002, 87 sea Iions Zalophus cali/ornianus were found lying or dying on the beaches between the border with USA and Ensenada, Baja California, and they are assumed to be poisoned by domic acid. California anchovy is considered to be the vec-

tor of domoic acid to its predators as birds and marine mammals

HABs in the Gul/of Ccrliforma

"Red Tides" are historical, frequent and periodical events in the Gulf of California, most of them are innocuous and produced by theciliate Myrionecrarubra(widely distributed in the Mexican Pacific: from Punta San Hipolito -27" N, 114' W- to Oaxaca -15: 4VN, 96"30' W-), but it is perhaps in Mazatlan, where historical and intensive records and studies have been done in the Mexican Pac i f i~ . [ ' ~~~ '~ The highest number of blooms is recorded for Mazatlan and La Paz. Some patterns of bloom occurrence in Mazat- Ian shows Gytrmoditriunr carenarwn appearing by March- April, Akashiwo sanguinea by May-June, aud Codrlodbrirur~ polykrikoides by September-October. Dinoflagellates may form considerable blooms with up to 20.45 x lo6 cells L-'.

Almost all main types of marine biotoxins produced by HABs in the world also occur in the Gulf of California: PSP, DSP, ASP, CFP, and other toxins as tetrodotoxin, conotoxin and freshwater toxins as the microcystins and others orgauisms types[44] Fauna mortality in the Gulf of California includes whales, seals, dolphins, pelicans, turtles and fishes among others One important eveut was the mortality of sea lions, dolphins and turtles close to Mazatlan Bay in 2003, during red tides of Gynmodb~iunr carwarwn. Gymnodiniwn i~rrrriarwn and Pseudo-nitisclzia spp. Events of mass mortality of fishes happened in several localities in Sinaloa and Sonora during Charrotrella spp. bloomsl"1 Fish mortality is common on Cochlodiniwn spp. blooms in coasts of Sinaloa.

During the last 10 years. the mariculture in Mexico has faced some problems due to HABs Mariculture basically consists in shrimp production and an incipient fish culture activity in the Gulf of California. Numerous cases of diseases, shrimp mortality and other problems associated to toxic and harmful phytoplankton have happened in the East of Gulf of Calif~mia!~'] Shrimp mortality associated to phytoplankton blooms in hatcheries and ponds has been reported since 1997,[''1 and in subsequent cases, Gymnodiniwn carenarwn blooms were occurring in the water supply during these mortality Other common cause of mortality of shrimp in culture is the anoxia caused by high densities of phytoplankton in the ponds. Previous conditions for forming blooms are often nutrients in ex- cess, changes in salinity, daylight time, wind or the income of sewage waters waters. Fish culture has already experienced the erects of HABs Since 2002, the red tides formed by Cochlodirriwnpolykrikoides in the coast, in natural and culture cause the c.a. 3Phof fish mortality?']

HABs in the Central Mexican PacjFc

Since 1986, systematic observations on HABs have been made in Manzanillo Bays, Colima. From 1999 there has

Phytoplankton and HAB microalgae in Mexican Coasts 1357

been a marked increase of thex HABs both in distribution Technical mdmethodolo~ical advmces and duration.[7n] In this area, 10 dinoflagellates dominate "red tides," but also two potentially harmful dinoflagellates, two diatoms, one silicoflagellate and one ciliate have been recorded. Higher densities of phytoplankton reached to more than 2 x lo6 per liter, however, no records of poisonings or toxin were made. From the dominant species recorded in Manzanillo Bays, Codilodutiunr polykrikoides has been the most recurrent and abundant. with its blooms occurring during March and April. Maximum bloom inten- sity in terms of time and extensions coincided with water temperatures between 21°C and 23°C and salinity ranging from 34.56 to 34.68. The location of HABs reported for Bahia Banderas and Mazatlan Bays agreed ~e11!~~]

The composition of potedally harmful dinoflagellates has been recently studied in coasts of Mi~hoacan.[~~] This study includes the species: Akoshiwo sanguinea, Ale.xon- drium carenello. Antylax rriacanrlza, Cerariunt furco, C. di- varicorunt var halcchii, Dinophysis coudoro, D. forrii, D. mirra, Gamhierd~~cus roxim, Gotzyaulax polygramma, G. spinifea, Gytnnodinium insrriorwn, Lingulodiniutn polye- dm, Nocriluco scitlrillmu, Prorocettrrunz miconr, P. rri- esrinum, Pvoroperi&ium crossipes, Scrippsiello rrochoideo.

HABs in Southern Mexicm Pacific

Apart from the records of HABs caused by P hohonrcnsc var. compressutn, there are few studies on other potentially harmful planktonic and epibenthic microalgae in the Gulf of Tehuantepec. Phytoplankton species composition has been studied in that area,["I and more recent reports indicate the presence of 24 "red tidesw-forming species, from which four taxa are important, the diatoms Skeleronema cosrarum complex and Pscudonir:schio delicorissutlo complex, and the potentially toxic dinoflagellates Alexmzdriunt acorenello and A. romorense, with their maxima densities reaching to 1.1 x lo5 and 2.2 x 10' cells L-I, in May, 2004 and January, 2005, for thediatoms, and 5.55 and 6.14 x 10' cells L-' by summer, 2006 for the dinoflagellates (Baron- Campis, comm. pers.).

Perspectives MCI future studies

Technical tnnovations to improve our understanding of HABs are needed, including integrated techniques to envis- age physical, chemical and biological variability. In Mexico, we would need long term monitoring programsthat can indicate certain tendencies of HABs and how they as- sociate with human activity. Opportune detection would also help to protect areas dedicated to aquaculture and may serve as a signal to justify other investigations aimed at characterizing together the distribution and physio- logical stage of the phytoplankton in an oceanographic

Positive identification and counting of phytoplankton cells are a fundamental issue in studying HABs, for toxic and harmful events are specific-species (e.g., species produce specific toxins or may not be toxic at all, even if they are responsible for "red tides"). Traditional and classic methods include the analysis of water samples by microscopy (either conventional or inverted microscopes). However, well-trained personnel and time for confident analysis are badly needed, because often quick results are necessary to take important decisions (e.g., determining whether or not the bloom may he toxic, mitigation plan). Technical ad- vances have contributed to less time-consuming analysis, as for example the incorporation of the Flow Citometry to biological 0ceanogra~h~.['~1 Study of resting stages (ha- sically cysts produced by many dinoflagellates) is an ap- proach to investigate possible distributioil and blooming of certain species Only recently, this study has started in M e x i ~ o . ~ ~ ~ . ~ ]

Pigment signatures are closely related to phytoplankton species composition, and specific pigments (also often termed "fingerprints") might he useful in HABs monitor- ine roer rams!^^^^^] This aooroach is oossible with new de- veTdpmints in High ~erfoimaoce ~ iqu id Chromatography (HPLC) technia~es!~'.~~l Most s~ecies forming blooms either toxic or not in Mexican watkrs (especially-in the Mex- ican Pacific) have pigment Vertical and temporal distributions can now be determined following this method.

For toxin analysis, there are numerous methods using Thin Layer Chromatography, HPLC, capillary elec- trophoresis, mass spectrometry, fluorimetry, or molecular tool^!",^^.^^] although the mouse bioassay is an established method, which is the "official" method for some author- ities and countries, and continues to be used in many laboratories.

Molecular tools have become very important to study HABs Molecular probes to potentially toxic species, which are very often difficult to Identify by conventional micro- scopical methods, are now widely used world~ide!~~-~'I an^ species of the genera Pseudo-nirzschio, Alexandrium and Chorrotiella, show morphological characters only oh- served in detail by electron microscopy in many cases, and are now routine monitored using this technique. Other detection and counting methods include use of lectins and antibodie~!~~1

Remote sensing instruments utilize electromaguetic ra- diation to study surface processes on earth, and various advantages of this method are accessing dilticult locations, rapidly mapping and a panoramic The ocean color imagery commonly used for studying HABs is produced from SeaWiFS estimates of surface Chl oconcentrations. Usins a sophisticated radiometer of a very high resolution and satellite equipment, Aguirre-G6mez et al!") recorded successfully the evolution of a HAB episode in the Mazatlan Bay.

Monitoring and mawgement progmms: toxins ~dphytoplankton

Health Ministry (Secretaria de Salud) through the "Comisi6n Federal para Riesgos Sanitarios" (COFEPRIS -Federal Commission for Sanitary Risks-) and State sanitary jurisdictions in Mexico, with the support of other insti- tutions ofthe Federal government, launched since 1984 the "Programa Mexicano de Sanidad de Moluscos Bivalves" (PMSMEMexican Program of Bivalve Moluscs Sanity), with the purpose of monitoring toxin levels in "red tide" or blooms events, mainly using the mouse bioassay method and taking adequate procedures to avoid human poisonings. Phytoplankton and toxins sampling by the INP has k e n done since 1996, however these activities were sus- pended from 2003. Since 1996 COFEPRIS coutinues monitoring "red tides" and their impacts by K. brevisinTamauli- pas, Veracmz and Tabasco. Historical records are found in the web site: (http://www.cofepris.gob.mx/marea Roja).

In Yucatan, the "Programa de Monitoreo de Florec- imientos Algales Nocivos" (Monitoring Program of HAB) was launched since 2000, with the participation of the Oceanographic Research Statiou of Progreso (Secretaria de Marina) and CINVESTAV-IPN, Unidad Mkrida. More recently, remote sensing imagery is used as an addi- tional tool for this purpose, with the "in real-time" added component.

Other program established nation-wide is the Red Tide Surveillance Program, through the web of Centros Tec- ~~ologicos de Mar (CETMAR) with 36 small centers, depending of the Direcci6n General de Estudios en Ciencia y Tecnologia del Mar de la Secretaria de Educaciol~ Publica (DGECyTM, SEP), which started in 1998, to investigate and inform on the events in Mexican coasts. There is a web site that gives general information and recent records: (http://fanscicese.mn).

In the southern Mexican Pacific, since 1998 there is a Surveillance and Monitoring Program of HAB's in CETMAR No. 24 (Center of Marine Technologic Stud- ies), at Puerto Madero, Chiapas, in a fixed station, three km off the coast (14'42'43"N and 92-25'08"W). Mouse bioas- says are also regularly made. This established monitoring allowed to follow presence and abundance of cysts sus- pended in the water column, preceding the vegetative cells of the blooms by Pyroduiiunr baha~ncruc vat. comprcssuni. in 200 1-2002 and 2006, and it has greatly aided evaluatio~l of saxitoxins and consequent fisheries banning.@'l

Monitoring in the central Mexican Pacific considered phytoplankton and chlorophyll a collected form surface water and CTDcasts performed at the same stations. HABs spreading have been detected by satellite data to prepare maps of SSC distribution between 21.4"-17' N and 101"- 109' W. These maps were used to detect possible bloom areas and their extension. The resulting SSC maps were projected with a resolution of 1 km, and a scale ranging form 0 to 20 wm L-l.

Collaborative appmahs

A formal evaluation of HABs impact in Mexico is not available, although an increase in number, periodicity, and impact of HABs is widely recognized. National newspa- pers have reported locations such as La Paz, Mazatlin, Manzanillo, Acapulco and Huatulco frequently stricken by HABs, but they do not mention the socioeconomical cost involved. Nevertheless, because of the lack of an appro- priate and systematic monitoring system, scientific records about HABs in Mexico are scarce.lR61 Only 2 certified labo- ratoriesauthorized by theHealthMinistry areable todetect toxins in mollusk samples. With a coastline of about 11,600 Km, this capacity is obviously insufficient to provide an opportune warning and assistance for HABs off coast of Mexico. The official records of the last 22 years indicate at least 500 cases of hospitalization and 20 casualties, which may be just the tip of a formidable iceberg of HABs health impact in ~ e x i c o . [ ' ~ ~ ~ ' ~

Aquaculture, fisheries and even tourism are strongly affected by HABr Thenoticeablesynchrony in theoccurrence of d~fferent HABs of Pyrodutiunt in the Central American Pacific. from Costa Rica to Mexico, suggested that they represent a regional e ~ e n t . [ ~ ~ l A formal regional project has started involvir~g phytoplankton researchers and persouuel of Health department in Central American countries, including Costa Rica, El Salvador, Guatemala and Mexico (States of Chiapas, Oaxaca and Guerrero), with the purpose of analyzing oceanographic and environmental variables' features related to the occurrences of blooms and their toxicity.

Only multinstitutional and multidisciplinary approaches to study HABs may guarantee a better understanding of the mechanisms and processes that lead to developing and keeping HABs, the possiblecauses and factors that enhance these phenomena, the role of human activities in thecoastal zone, the responses of species involved, possible trends and seasonality, biology andecophysiology (includinglifecycles and life histories), and the possibility of developingaccurate methods to forecast their occurrences.

Local and global factors

Increase of cases of HABs in the world and Mexico are currently related to various factors, most of then of anthropo- logic origin: rapid increase of human population, increased utilization of coastal waters for aquaculture. cultural eutrophication and pollution, transport of resting stages (cysts, resting spores) in ships' ballast waters;[' '~m~87.881 different hydrographic conditions, global climatic ehange and unusual climatologic conditions (leading to a wide range of global, regional and loeal ell'ects: oceanographic patterns, rain regimes, E1Niio SouthernOscillation-ENSCbevents) are also involved in "stimulation" of algal blooms at local and global scale.['-'~"l An important amount of information proceeding from monitoring, xientifie research and

Phytoplankton and HAB microalgae in Mexican Coasts

collaboration is still required to propose mitigation policies conducing to reduce risks in health and economic losses

Coastal eutrophication in the north of Yucatan represents a big environmental problem.[89,"l The increase of ammonia and urea due to waste water may promote blooms of toxic and harmful species, replacing other phytoplankton species that regularly occur there. Evidence of blooms caused by innocuous species, such as Ditylunr brightwelli and species of Bacteriastrum, Guinardia, Leptocylindrus, Ornifltocer- cus, Pleurosign~a, Proboscia. Protoperiduiiunt, Rhitosolenia, that precede HABs, may be used as an indicator of their imminent appearance and also to establish their temporal occurrence in Yucatan. This fact, together with oceanographic processes such as upwellings, seems to contribute to the developing of HABs.

Sufficient evidence exists that eutrophication has accel- erated in Mexican coastal waters, and we still need to know how this can aid HABs developments. For instance, we speculate that the increase of HABs in Manzanillo Bays, Mexican Pacific, is associated to the increased activities of the port. On the other hand, in the area of Mazatlan bay, also in the Pacific, the waters are mostly eutrophic, with presence of red tides close to the submarine waste water d i~ t r ibutor . l~~]

Introduction of potentially harmful species is a mecha- nism that has been proposed for the reamt finding of the naked dinoflagellate Cochlod~iwnpolykrikoides,[71] of wide distribution in the Mexican Pacific, which was only observed from 1999 in Manzanillo, Colima!"'l and no previous record in Mexican waters[10] The hypothesis includes ships' ballast waters.

We have a general understanding of the movement of biotoxins through the food chain. Some blooms initiate offshore in more oceanic zones: microalgae increase in number as the bloom is moved toward shore, driven by wind and currents The bloom is initiated and sustained by upwelling in the continental shelf, which brings up cooler water rich in nutrients required by the cell for reproduction. Small pelagic (herbivorous fish), such as anchovies and sardines, consume phytoplankton, accumulate toxin iC it is present, and they in return pass it onto predator species such as marine mammals or humans. On the other hand, benthic filter feeders (bivalve mollusks: mussels, clams and oysters) also accumulate toxins It is necessary to quantify the toxin pathway through food net to obtain better models.

oce~ographic and climatic processes

Upwelling events are usually short-time events Some local and regional phenomena regarded HABs are undoubtly related to their patterns in some areas (e.g., western coasts of Baja California, the Gulf of California and the Gulf of Tehuantepec). We have to gain knowledge on the mecha-

nisms that regulate blooms in these areas and also the role of post-upwelling periods and mixing of waters in adjacent. In coasts of Yucatan, HABs seem to be associated to upwellings from the Mexican Caribbean, which come to the Gulf of Mexico, bordering the northern coast in the State. The different types of water combined may favour microal- gal blooms.

In Manzanillo Bays, an invcrse correlation was found between surface chlorophyll a and temperature. There is a remarkable spatialdistribution in red tides: one bay showcd red tidecaused by one species, whereas the other wascaused by another species or showed no event. The observed increase of HABs between 1999 and 2000 in the Pacific Mex- ican coastal zones coincided with the lowest temperatures recorded in the area and was probably related to the neg- ative anomalies of temperature encountered in the North Pacific Ocean during the period of La Niiia 1999-2000.

El Nido (ENSO) plays a complex role in plankton biomass variation along the Peninsula of Baja California, the Gulf of ~ a l i f o r n i a ! ~ ~ ~ ~ ~ ] and the Gulf of Mexico and the Mexican Caribbean. El Nifio seems to cause a decline in upwelling-based primary productivity along the western coast of Baja California. In contrast, in the mouth of the Gulf of California, temperatures above the nornlal (29- 30'C) attributed to the presence of El Nido, favour the replacement of nutrient-rich waters by oligotrophic waters causinga very low productivity. Thestrong tidalmixingand upwelling events that tend to mask the effect of such a climatic phenomenon should be considered to draw any con- clusion about the El Nifio influence in primary productivity in the Gulf of California. Gonzalez-Lope~~~~] a~sociatedl'~1 El Niiio events in the Gulf of California, identifyin&18] phytoplankton species to find "markers"

El Nido and HABs incidence in coasts of Mexico is, however, not yet clear. Cortts-Altamiranolw reported that El Niiio favours the development of some blooms in Mazatlan Bay, but not in the Gulf of Also Manrique & MolinalWl have found an inverse relationship between El Niiio and HABs occurrences in the Gulf of California. Thc analysis of 43 cases of HABs during the last 25 years by these authors point out to Noctiluca scinrillnns, Gymno- duziunz catena tun^, Lit~guloduriuntpolycdra and Miryorwcra rubra as dominant species, with no evidence of toxicity during blooms occurring in November, December, and Hn- uary each year. The diatom Pseudonbrzchia awrralis a ~ ~ d the toxin domoic acid were detected in bodies of stranded animals in Sillaloa beaches derived from a mass mortality of sea-birds,fish, and seamammals, duringa strong El Nido event. As it appears. El Niiio. with the exceptions of 1976, 1984 and 1997 events, generally attenuates the blooms in such an areaI94

The occurrence of the El Niao events seem to be more frequent and intense: the 1997-1998 EL Nifio and 199% 2000 La Nifia were the most intense on record, showing evidenceofclimaticchange and its impacts. Theexceptional HABs recorded in coastal line and offshore in Mexican

Central Pacific Watenduring the 1999-2000La Nifiaevent, might give an orientation towards what could be with the recurrent presence of this events in the area.

Appmaching new concepts a n d p a m d i g m

The recent established concepts about the term "species" should be considered from now on in studying HAB. Concepts like "species complex," "cryptic (and semicryp tic) species'' and morphological and genetic variation of species require actualization, discussion and new research proposals. Athecate dinoflagellates (Karerria, Karlodiniunt, Takayama), and species of many thecate genera (with a potential thread to the environment in terms of invasion, toxicity and harm) such as Alexandrium, Gambierdiscur. Hererocapsa, Scrippsiella are poorly known in Mexico, and recent proposals of "cryptic species" of the diatoms genera Pseudonirzschia and Skeleronmria[9'-96] call for further studies on morphology and taxonomy of these groups.

A particular issue to be investigated is the identity of Pyroduriunr bahanrense var. hahantense and its relationship to the var. compressurn in the Mexican Pacific. The former has been detected since 1942[971 andmore Vargas & Freer'"] found both taxa in an extensive bloom in 2001, in Costa Rica: they believed both taxa correspond to stages in the life cycle of a given taxon.

Mixed species and the synergic have heen much less studied in Mexicall waters: the only available example is the finding of certain species associations, such as Cer- ariunr Jurca-Prorocentrwn nricans. Alexmrdriunr carerwlla, Dinophys;.~ a c u n r i n a r ~ . [ ~ I

An important issue that has not been dealt with is the knowledge of the biology of the species involved in HABs In Mexico we know few details of the physiology and ecol- ogy, life cycles life histories, cyst or resting stages production, range of environmental conditions of causative species of HABs More detailed studies should be made on the proposed evolutive strategies that seem to givecom- petitive advantages to many of the HABs species. Some of them were summarized by S ~ n a ~ d a : [ ~ ~ I (1) nutrient retrieval migrations, (2) mixotrophic tendencies (3) allelopchemi- cal competition, and (4) allelopathic, antipredation defence mechanisms. These studies imply ecophysiological research both in the field and experimental, controlled conditions.

The low toxicity of regional strains needs to be studied by molecular techniques. We do know the relationship between algal growth and toxin production depending on nutrients (silicates different nitrogen sources, phosphates, perhaps iron), organic matter (e.g.. vitamins) and temperature. The precise values for predictive models, has yet to be developed. In related fields histopathologic studies of the acute and chronic exposition to PSP and NSP toxins are currently being developed, based on the model of mouse, and toxin accumulation and deputation in shrimp. Toxic- ity and biological activity of Antphiditriunt carteroc, Cochlo- duriuntyolikrikoides. Gymnodiniunt carenatwtt, Karenia bre-

vis. Prorocenrrum limo, P . minimum. Prorocenrrwn sp., P.v- rodhiunr h a h a n r e ~ u e var conrpressunr are current subjects for investigation!"I These investigations may eventually contribute to redefine the Norma Oficial Mexicana (Offi- cial Mexican Norm) with regards to toxicity levels in marine products to human consumption.

Acknowledgments

Thanks are due to Maru Zamudio for Constructing Figure I (map).

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Toxic and harmful marine phytoplankton and microalgae (HABs) in Mexican Coasts