Unusual Mortality of Krill (Crustacea: Euphausiacea) in Bahıa De La Paz

Unusual Mortality of Krill (Crustacea: Euphausiacea) in Bahı´adeLa Paz, Gulf of California1

David J. Lo´pez-Corte´s,2 Jose´ J. Bustillos-Guzma´n,2 and Ismael Ga´rate-Liza´rraga3

Abstract: Surface aggregations and beach strandings of a species of krill, Ne- matoscelis difficilis Hansen, were observed in June 2003 at locations along the shore of Bahı´a de La Paz in the Gulf of California. For 10 days before the krill die-off, a steady wind blew from the south at speeds between 4 and 5 m/sec. For that period, satellite images showed water temperatures between 18 and 22 C along this coast, which is low compared with typical seasonal water temperatures of 26 to 28 C for June. Phytoplankton biomass, determined by pigment con- centration and cell counts, was the highest in the area in June. The diatom Chaetoceros debilis represented more than 96% of the phytoplankton community. Nutrients were in relatively higher concentrations. These data suggest that upwelling conditions occurred and the diatom bloom was in its final phase. Based on this limited data set, we present a hypothetical scenario describing the sea-surface aggregations and beach strandings of N. difficilis.

The euphausiid or krill species Nematoscelis ponent of the zooplankton fauna (Boden difficilis Hansen is distributed in the northern et al. 1955, Go´mez-Gutierrez 1992, De Pacific Ocean in the transitional zone (30–45 Silva-Da´vila et al. 2002). In Bahı´a de La Paz, N) of the North Pacific Drift and California a large bay in the southwestern part of the Current (Brinton 1962). Vertical distribution Gulf of California, N. difficilis has been re- of N. difficilis is typically between 100 and corded for several years but only in deep 200 m (Brinton 1967). In the Gulf of Califor- zones and at low densities. Aggregations nia and along the Pacific coast of the Baja described for other krill species, such as Nyc- California Peninsula, it is present in many lo- typhanes simplex (Gendron 1992) and Nycty- cations and seems to be a conspicuous com- phanes australis (O’Brien et al. 1986), have not been recorded for Nematoscelis difficilis. In June 2003, several surface aggregations of 1 Partial financial support was provided by CIBNOR N. difficilis were observed, lasting for several Projects PC 3.2 and PC 3.3 and Secretarı´a de Medio days. Because this euphausiid inhabits deep Ambiente y Resursos Naturales–Consejo Nacional de Ciencia y Tecnolo´gia (SEMARNAT-CONACyT) (grant waters (Brinton 1967), these aggregations 2002-COI-0318-A-1). Other financial support came from near and on the beach made us suspect a rela- the Instituto Polite´cnico Nacional (grant CGEPI tively rare event. We describe this event here 20040626). I.G.-L. received a fellowship from the Comi- and, supported by a small data set of physical, sio´n de Cooperacio´n y Fomento de Actividades Acade´mi- cas (COFAA) and from Estı´mulos al Desempen˜ o de los chemical, and biological observations, specu- Investigadores (EDI). Manuscript accepted 13 June 2005. late about the causes of this phenomenon. 2 Centro de Investigaciones Biolo´gicas del Noroeste (CIBNOR), Mar Bermejo 195, Col. Playa Palo de Santa materials and methods Rita, La Paz, Baja California Sur 23090, Mexico (e-mail: [email protected]). 3 Departamento de Plancton y Ecologı´a Marina, Cen- Euphausiid surface aggregations were ob- tro Interdisciplinario de Ciencias Marinas (CICIMAR- served in June 2003 in Bahı´adeLaPaz IPN), Apartado Postal 592, La Paz, Baja California Sur (@24.5 N, 110.5 W) at several locations 23000, Mexico. (Figure 1). Organisms were in bands about 100 m wide and 1,000 m long, separated 300–400 m from each other. These bands Pacific Science (2006), vol. 60, no. 2:235–242 2 : 2006 by University of Hawai‘i Press covered approximately 60 km on the All rights reserved southern and eastern coast of the bay as well

235 236 PACIFIC SCIENCE . April 2006

Figure 1. Location of the study area, where an unusual mortality of krill Nematoscelis difficilis occurred in June 2003.

as 15 km2 on the southern part of the Ense- tion and cell counts. Cell counts were made nada de La Paz, the lagoon located at the in 5-ml settling chambers using a phase- southern end of the Bahı´a de La Paz (Figure contrast inverted microscope (Hasle 1978). 1). Samples were collected in 1-liter plastic Phytoplankton abundance was estimated at bottles directly from the aggregations and the same time as identification of species fixed with 10% buffered formalin. Water using sedimentation chambers in an inverted samples were taken with Van Dorn bottles to microscope (Zeiss). Sea-surface temperature determine nutrient concentrations (NH4, was measured with a bucket thermometer NO3,PO4, SiO4), pigments, and abundance (Kahlsico International Corp., El Cajon, Cal- of phytoplankton and planktonic species. ifornia). Nutrients were measured according Also, two samples of phytoplankton were to Strickland and Parson (1972). Chlorophyll fixed and preserved with Lugol for identifica- was identified with HPLC (high-peformance Unusual Krill Mortality in the Gulf of California . Lo´pez-Corte´s et al. 237 liquid chromatography) (Vidussi et al. 1996). the appearance of surface aggregations of Identification and assessment of abundance krill in 2003, winds were blowing from the of chlorophyll pigments were performed as south at speeds as high as 4 to 5 m/sec for described in Bustillos-Guzma´n et al. (1995). 10 consecutive days (Figure 3). The wind di- Meteorological data were obtained from the rection, duration, and intensity could create CIBNOR meteorological station located 200 conditions for mixing shallow water with m from the southwestern shore of the Ense- deeper layers, thereby decreasing surface nada de La Paz. temperatures (Go´mez-Gutie´rrez et al. 1999). Seawater was brownish from high phyto- results and discussion plankton density and pigmentation. Phyto- plankton density in the samples ranged from Nematoscelis difficilis aggregations, composed 1.24 to 1:35 Â 106 cells literÀ1. High chloro- of dead (95%) and live (5%) organisms on phyll a (557.0 mg mÀ3) and fucoxanthin the sea surface and forming rows several hun- (228.2 mg mÀ3) content was present, together dred meters long, lasted several days. Density with other minor pigments (Table 1). Jones of krill was about 300–320 specimens per et al. (1982) described a red tide of Gyrodi- liter. This pattern may be a consequence of nium aureolum in western Scotland that vortices, called Langmuir Circulation, set up reached a biomass as high as 2,200 mg mÀ3. by a continuous wind in relatively calm seas. Fucoxanthin is a pigment characteristic of On the beaches, several slightly elevated diatoms (Liaeen-Jensen 1985). The biomass bands linked to tide levels and small ponds and species composition confirmed that the with dead krill were also present. phytoplankton bloom was largely diatoms, Of seven euphausiid species previously re- particularly Chaetoceros debilis, representing ported in the Bahı´a de La Paz, Nyctiphanes >96% of the phytoplankton community, simplex is the most abundant, followed by N. with densities >1 Â 106 cells literÀ1 (Table difficilis and Euphausia distinguenda. Nematosce- 2). This is the highest concentration recorded lis difficilis usually occurs in deeper waters be- in this area, even when compared with values tween 100 and 200 m and is considered a obtained during other algal blooms (Ga´rate- transitional oceanic species with a composi- Liza´rraga et al. 2001, 2003, 2004). Zooplank- tion of a maximum of 1.4% larvae (all stages) ton in net and bottle samples was very scarce, and over 98% adults (De Silva-Da´vila 1997). suggesting low grazing activity. These fea- On this occasion, our samples showed only tures suggest that a diatom bloom was oc- one krill species, N. difficilis, with less than 2% curring during the occurrence of the krill larvae. Krill containing parasitoid ciliates, as mortality. However, nutrient concentrations described by Go´mez-Gutie´rrez et al. (2003), (Table 1) were similar or at relatively higher was not present. This krill occurred in the concentrations than those previously reported southernmost, shallow part of the bay, in- for the area (Reyes-Salinas 1999, Cervantes- cluding the Ensenada de La Paz, an unusual Duarte et al. 2001, Ga´rate-Liza´rraga et al. situation. Here, the sea-surface temperature 2004). It is probable that fertilization oc- ranged from 18 to 18.5 C. This is a low tem- curred before the krill die-off, and species perature compared with typical seasonal tem- with high nutrient affinity, such as diatoms peratures of 26 to 28 C for this month (De (Smayda 1997), had exhausted the nutrients. Silva-Da´vila et al. 2002, Reyes-Salinas et al. Therefore, the die-off occurred during the fi- 2003). Satellite images show a temperature nal stage of the bloom. Although, we did not range from 18 to 22 C along the Bahı´ade measure oxygen concentration, it is plausible La Paz when krill mortality occurred (Figure that under the conditions described here hy- 2). During summer 1981, similar low temper- poxic or anoxic conditions below the euphotic atures (@18 C) were recorded in this area zone can occur from oxidation of organic (Granados-Guzma´n and A´ lvarez-Borrego matter, as suggested by Lechuga-Deve´ze 1983), and this was attributed to upwelling et al. (2001). waters from the Gulf of California. Before A scenario of the physical, chemical, and Figure 2. Sea WiFS images showing temperature variations in Bahı´a de La Paz in 2003: (A) 23–30 May composite image, (B) 5–12 June composite image, and (C) 23–30 June composite image. Sea-surface temperature maps were obtained from the CoastWatch program (National Oceanic and Atmospheric Administration). Unusual Krill Mortality in the Gulf of California . Lo´pez-Corte´s et al. 239

Figure 3. Speed (A) and direction (B) of the winds from 20 May to 20 June 2003 in the Bahı´a de La Paz. Bold hori- zontal line shows the 10-day period before N. difficilis mortality. Wind direction is given in degrees.

TABLE 1 Photosynthetic Pigment and Nutrient Concentrations during the Unusual Mortality of Nematoscelis difficilis in 2003 in Bahı´a de La Paz, Gulf of California

Pigments (mg mÀ3) Nutrients (mM)

Chlorophyll a Fucoxanthin Peridinin Chlorophyll b NH4 NO3 PO4 SiO4

557.0 228.2 1.54 18.6 7.35 4.48 1.36 4.58

biological characteristics and circumstances led to a decline of available nutrients. A related to the mortality of this krill is sum- decoupling of primary production and zoo- marized as follows. Prolonged winds from plankton grazing may have occurred, as sug- the south (Figure 3) provoked fertilization gested by the low density of zooplankton. of the euphotic zone by resuspension of nu- As the organic matter produced at the sur- trients from the shallow areas and upwelling face sank below the compensation depth of nutrient-rich waters from below the ther- (Sverdrup 1953), depletion of the oxygen in mocline. This promoted a massive increase the water column and the bottom occurred. of phytoplankton. Phytoplankton production Organisms inhabiting euphotic and bottom 240 PACIFIC SCIENCE . April 2006

TABLE 2 Phytoplankton Species Recorded during the Bloom of June 2003 in Bahı´a de La Paz, Gulf of California

Species Sample A (cells literÀ1) Sample B (cells literÀ1)

Diatoms Asteromphalus heptactis (Bre´bisson) Ralfs 200 0 Azpeitia nodulifera (A. Schmidt) G. Fryxell & P. Sims 200 0 Chaetoceros debilis Cleve 1,300,000 1,196,000 Cocconeis scutellum Ehrenberg 0 400 Leptocilyndrus danicus (Cleve) 1,200 1,800 Lyrella lyra (C. G. Ehrenberg) N. I. Karayeva 0 400 Planktoniella sol (Wallich) Schu¨tt 200 0 Rhizosolenia debyana H. Peragallo 400 0 R. imbricata Brightwell 800 0 Thalassionema frauenfeldii (Grunow) Hallegraeff 2,400 4,000 T. nitzschioides (Grunow) Mereschkowsky 24,800 32,400 Dinoflagellates Ceratium furca (Ehrenberg) Clapare`de & Lachmann 1,000 200 Gonyaulax polygramma Stein 1,200 0 Gymnodinium catenatum Graham 1,200 800 Phytoflagellates 16,200 8,400 Total phytoplankton abundance 1,349,800 1,244,400 zones, as is the case for N. difficilis, were acknowledgments forced to migrate to more-oxygenated sur- face waters. Surface currents carried the or- The editor at CIBNOR provided much im- ganisms to the shallow parts of the bay and provement to the English text. Thanks to ´ lagoon. Once the organisms were at the sur- Maria Clara Ramırez-Jauregui (Instituto de ´ face, wave action deposited the flotsam on Ciencias del Mar y Limnologıa [ICMyL], Universidad Nacional Auto´noma de Me´xico the beach. In another report, Nyctiphanes sim- [UNAM]) for the literature search and to plex was the dominant species during a mas- sive mortality event near Guaymas, Sonora, two reviewers for their comments and sug- Me´xico (Montemayor-Lo´pez and Cisneros- gestions. Mata 1999). Those authors suggested that Literature Cited the massive die-off of that species was related to the 1997/1998 El Nin˜ o. In Chilean coasts, Boden, B. P., M. W. Johnson, and E. Brin- stranding of krill species Euphausia mucronata ton. 1955. The Euphausiacea (Crustacea) is apparently common and associated with of the North Pacific. Bull. Scripps Inst. upwelling conditions (Melo 2003). In our Oceanogr. 6 (8): 287–400. study, we hypothesize that mortality of N. Brinton, E. 1962. The distribution of Pacific difficilis was related to cooling of seawater af- euphausiids. Bull. Scripps Inst. Oceanogr. fected by unusual meteorological conditions, 8:51–270. including generation of cold-water upwelling. ———. 1967. Vertical migration and avoid- Monitoring programs directed toward harm- ance capability of euphausiids in the Cali- ful algal blooms or detection of zooplankton fornia Current. Limnol. Oceanogr. 12: aggregations will probably provide more ob- 451–483. servations of plankton blooms in this area Bustillos-Guzma´n, J., H. Claustre, and J. C. and their ecological consequences. This will Marty. 1995. Specific phytoplankton sig- lead to a better understanding of phytoplank- natures and their relationships to hydro- ton blooms and zooplankton swarming under graphic conditions in the coastal north- various conditions and of the mechanisms western Mediterranean Sea. Mar. Ecol. that trigger and sustain a particular bloom. Prog. Ser. 124:247–258. Unusual Krill Mortality in the Gulf of California . Lo´pez-Corte´s et al. 241

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