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Toxic algae in the Western Mediterranean: a new threat for the critically endangered Balearic Shearwater Puffinus mauretanicus

Authors:

Abstract

Massive strands of seabirds are always a cause of concern, particularly if involving threatened species and if no direct cause-effect relationship can be quickly established. The late concept is definitely influenced by the usual lack of quick response to these phenomena, with no fresh corpse processing or pluridisciplinary analysis (e.g. Shumway et al 2003).Establishing the causes of such events can help in future management of seabird populations. The arrival of 44 corpses of shearwaters to Roses Bay, Girona, NE Spain (figure 1) gave the opportunity to establish a chain of events with toxic algae as the lethal agent after such death episode.
Toxic algae in the Western Mediterranean: a new threat for the critically
endangered Balearic Shearwater Puffinus mauretanicus
Ricard GUTIERREZ*, Jordi MARTÍ-ALEDO, Robert MINOBIS & Maria PIFARRÉ*
* Servei de Protecció de la fauna, flora i animals de companyia . Dr.Roux, 80.08018-BARCELONA Contact: rgutierrez@gencat.net
Acknowledgements
To the personnel of the Natural Parc dels Aiguamollsof l'Empordà by its exemplary collaboration
during the episode, amongst them Àlex Ollé, Albert Burgas, Joan Ram on Sanz and Josep Espigulé. To
the personnel of the ACA, ICM and IRTA who collaborated with great interest in the episode. To
Miguel McMinn and Ana Rodriguez by its continuous support a nd interest. Jordi Ruiz-Olmo, Sergi
Sales, Francesc Carbonell, Josep Carda, Pierre Yésou and all the network of observe rs of the GIAM by
its collaboration in the monitoring of the case.
References
Arcos, J.M. & Oro, D. 2005 Pardela Bal ear Puffinus mauretanicus. En Madroño,A., González, C. & Atienza,
J.C. (eds). Libro Rojo de las Aves de E spaña. Dirección General para la Biodiversidad- S EO/BirdLife.Madrid.
Feliu, P. 2007 Baldriga Mediterrània Puffinu s yelkouan. Ornitho-Empordà. Noticiari OrnitològicMaig
2007.http://www.ornitho-emporda.cat/html/noticiaris/maig07.htm
Gutiérrez, R. 1998. Flight identification of Cory’s and Scopoli’s Shearw aters. Dutch Birding, 20: 216-225.
Gutiérrez, R. 2004. Identification of Balearic, Yel kouan and Manx Shearwaters. Birding World 17 (3):111-
122
Lefebvre, K.A., Silver , M.W., Coale, S.L. & Tjeer dema , R.S. 2002. Domoic acid in planktivorous fish in
relation to toxic Pseudo -nitzschia cell
Work, T.M & Rameyer, R.A. 1999. Mass stranding of Wedge-Tailed densities. Marine Biology140: 625–
631Shearwater chicks in Hawaii Journal of Wildlife Diseases, 35( 3): 487–495
Shumway, S.E, Allen, S.M., Dee Boersma, P. 2003 . Marine birds and harmful algal blooms: sporadic
victims or under-reported events? Harmful Al gae, 2: 1–17
Massive strands of seabirds are always a cause of concern, particularly if involving threatened species and if no direct
cause-effect relationship can be quickly established. The late concept is definitely influenced by the usual lack of quick
response to these phenomena, with no fresh corpse processing or pluridisciplinary analysis (e.g. Shumway et al 2003)..
Establishing the causes of such events can help in future management of seabird populations. The arrival of 44 corpses of
shearwaters to Roses Bay, Girona, NE Spain (figure 1) gave the opportunity to establish a chain of events with toxic algae
as the lethal agent after such death episode.
Background
After one week of strong northern winds (locally called tramuntana, figure 2) in the Cap de Creus area, with sustained gusts of wind of
up to 120 km/h, sport fishermen found different corpses of birds floating near the shore and stranded on the beach on Monday
21.5.2007. They turned out to be shearwaters floating on the South coastal sector of the Roses bay, Girona, where marine currents from
the north accumulated the corpses. On 22.5.2007 this phenomenon was discovered by the ornithologists of the Natural Park of the
Aiguamolls of l'Empordà that, in a section of 300 meters in the municipality of Sant Pere Pescador gathered 21 corpses of Mediterranean
Shearwater Puffinus yelkouan (figure 3). Once alerted the Wildlife Ser vice of the Government of Catalunya, and given the possibility that
there were more individuals of this one or similar protected species, a search throughout all the bay of Roses was organized. Twelve km
of the bay were scanned thoroughly between the 23 and 24.5.2007 and 41 corpses of Puffinus yelkouan, two of Balearic Shearwater
Puffinus mauretanicus and a single Scopoli’s Shearwater Calonectris diomedea diomedea were collected (figure 4 ). Species ratio
mirrored the 20:1 proportion of yelkouan/mauretanicus registered in the Roses bay the week before during a regular seabird count
(J.Martí-Aledo, own data).
Birds were identified according to recent identification criteria (Gutiérrez 1998, 2004) and biometric data was collected.
Corpses examination
Birds were in overall external good condition, without any visible cause of death. An autopsy of three of the fresher corpses was carried
out on 23.5.2007. The three birds were adult females with brood patch but inactive gonads. Death had occurred more than 48 hours
ago. All corpses showed a good body condition, with good muscle condition and average subcutaneous, cardiac and peritoneal fat
deposits. Lungs were not flooded, so the birds had not died by drowning. Despite internal organs of the birds were rather autholitic,
were apparently without visible anom alies. However, the gastrointestinal tract was comple tely full of small Clupeidae (anxovies and
sardines), from the stomach to the large intestine. Most of fishes were complete, suggest ing an early and quick death after its ingestion.
Causes of death
Five further corpses were derived to laboratory with the purpose of discarding any affectation of viral type, including bird influenza within
the framework of the passive monitor ing of this affection on operation in Catalon ia. This mortality cause was quickly discard ed.
The symptomatology and characteristics of the carcases took initially to the hypothesis of a sudden death by consumption of the
anxovies and sardines, well known vectors (e.g. Lefebvre et al 2002) of toxic marine seaweed of the Pseudo-nitzschia genus,
producers of domoic acid, of powerful neurotoxic effects. The Catalan Water Agency (ACA) of the Catalunya Government has a system of
control of the coastal waters in wh ich the monitoring of the coasts and these toxic algae is framed. The ACA, the Institute of Sciences of
the Sea of the CSIC and the IRTA, the Department of Agriculture, Feeding and Rural Action, collaborated with the Department of
Environment and Housing in the e lucidation of the case. Stomach contents and other remains of a part of the collected car cases were
analyzed. Toxin presence was detected in the body of corpses, indicative of a cause-effect nonregistered before in shearwaters but in
others of marine birds (e.g. Shumway et al 2003).
Further alert and overall impact
Given the possibility that some birds affected by this algae bloom could be moving towards other sectors of the Mediterranean, we
alerted the French, Balearic and Valencia g overnments as well as the network of observers of the GIAM (Iberian Group of Seawatchers).
During the following week certain movement of P.yelkouan in a southwards direction was observed along the coasts of the province of
Barcelona. In that context, two floating corpses of P. yelkouan were detected floating offshore, four miles in front of the coasts of
Mataró, Barcelona (Francesc Carbonell in litt.), presumably pertaining to the same episode, either died in situ or dragged by the
dominant north-south current of the zone. Taking into account of the number of shearwaters registered in the Cap de Creus/Roses areas
in the preceding weeks (6024 birds in passage by the Cap de Creus to the on 5.5.2007, historical maximum, Feliu 2007), it is reasonable
to think that the affectation to the birds in this episode could even be greater than the detected one.
Discussion
Although the poisoning by toxins in Pro cellariiformes would be a rare phenomenon and mor talities observed in beaches have been
usually attributed to other causes (e.g. Work & Rameyer 1999), the methodological difficulties in the investigation of the causes of
mortality that have required in this c ase the use of electronic microscopes for t he specific identification of the ph ytoplankton, and the
need of a multidisciplinary te am for this kind of investigations, further complicate the explanation of this type of events, that can happen
unnoticed or masked by other causes.
In spite of the ecological damage of this poisoning was serious, since all inv olved birds are protected species, we th ink it was an
exceptional event, favoured by the coincidence of a the northern wind tramuntana weather that removed the waters of the bay; the
presence of banks of young sardines and anchovies and the coincidence of a large mixed flock of these shearwaters in the zone.
This episode preceded a demographic explosion of toxic phytoplankton for humans in the coast of Girona, reason why the affectation in
birds could have been a case of early alert of other episodes. From May 2007 the Wildlife Service is in cluded in the network of toxic
seaweed monitoring of the Catalan coast.
The possibility of poisoning by toxic algae is an additional factor to all the elements that already widely threaten the Iberian
Procellariiformes and that have taken to classify for example the Balearic Shearwater as critically endangered of extinction (Arcos & Oro
2005). Therefore, the presence of toxic seaweed in strategic places for the conservation of the Procellariiformes has become a new
element of concern to be also considered for the conservation of these species.
Figure 1 Roses Bay, Alt Empordà, Girona, where the strand was recorded
Figure 2 Wind speed (m/s, blue) and direction (in degrees, red) at Cap de
Creus on 20th May 2007
Figure 3 Mediterrane an Shearwater Puffinus yelkouan
Figure 6 Mediterrane an Shearwaters Puffinus yelkouan
Figure 4 Post-mortem examination and biometry s ampling Figure 5 Beach survey and corpses collection
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In at least two mass mortality events in Monterey Bay, California, planktivorous fish were implicated as vectors of the neurotoxin domoic acid (DA) from diatoms to sea birds and marine mammals. Whereas the transfer of DA from planktivorous fish to piscivorous predators has been well established, the relationship between toxin levels in plankton-feeding fish and the regional abundance of DA-producing diatoms has not been documented. Here we present data from an extensive field study in which cell densities of toxic Pseudo-nitzschia species and DA levels in anchovies and sardines were measured from samples collected weekly throughout Monterey Bay from 8 October 1999 to 18 October 2000. Four distinct blooms were documented with cell densities ranging from 3.2쎷 to 5.0쎹 cells l-1. DA was detected in fish viscera samples whenever toxic diatom densities reached 䒟 cells l-1 in surface waters, suggesting that anchovies and sardines regularly consume toxic diatoms when present. Fish contained DA levels above the regulatory limit (20 g DA g-1 whole fish) only when toxic cell densities exceeded 104 cells l-1. DA was only detected in fish when toxic diatom species were also present in the water, suggesting that the toxin is quickly depurated and that fish are only dangerous vectors during the bloom period. Anchovies appear to be more potent vectors than sardines as they consistently contained more DA than sardines collected simultaneously. Maximum DA levels detected in fish were 1,815 g DA g-1 in anchovy and 728 g DA g-1 in sardine viscera samples. In fish with high viscera levels of DA, corresponding body tissues contained 0.2-2.2 g DA g-1 (0.2&#450.1% of the viscera level), suggesting that DA is not accumulated in edible body tissues to levels that threaten human consumers. Results from this study suggest that anchovies may be a valuable indicator species for assessing the risk of DA intoxication to piscivorous sea birds and mammals during toxic Pseudo-nitzschia blooms in Monterey Bay.
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From the late Pliocene to now, blooms of toxic algae are associated with mortalities of marine birds. Given the long historical presence of harmful algal blooms (HABs) worldwide and the numbers of seabirds that feed on filter-feeding fish and shellfish, it is surprising that relatively few incidents of seabird deaths as a result of toxic algae have been reported. The limited information available tends to come from major events, whereas the rare events are missed and hence not reported. Much is anecdotal and still more probably is not published. We suspect that factors working in concert may lead to deaths and wrecks that might not occur as a result of anyone factor working independently, e.g. starvation tends to render birds more vulnerable to stress.
Pardela Balear Puffinus mauretanicus
  • J M Arcos
  • D Oro
Arcos, J.M. & Oro, D. 2005 Pardela Balear Puffinus mauretanicus. En Madroño,A., González, C. & Atienza, J.C. (eds). Libro Rojo de las Aves de España. Dirección General para la Biodiversidad-SEO/BirdLife.Madrid.
Flight identification of Cory's and Scopoli's Shearwaters
  • R Gutiérrez
Gutiérrez, R. 1998. Flight identification of Cory's and Scopoli's Shearwaters. Dutch Birding, 20: 216-225.
Mass stranding of Wedge-Tailed densities
  • T Work
  • R A Rameyer
Work, T.M & Rameyer, R.A. 1999. Mass stranding of Wedge-Tailed densities. Marine Biology 140: 625631Shearwater chicks in Hawaii Journal of Wildlife Diseases, 35(3): 487-495