Impact of Two “El Niño” Events of Different Intensity on the Hypoxic Soft Bottom Macrobenthos off the Central Peruvian wast

P.S.Z.N. I: Marine Ecology, 17 (1-3): 425-446 (1996) 0 1996 Blackwell Wissenschafts-Verlag, Berlin ISSN 0173-9565

Accepted: May 17, 1995

Impact of Two "El NiAo" Events of Different Intensity on the Hypoxic Soft Bottom Macrobenthos off the Central Peruvian wast JUAN TARAZONA~, WOLF E. m2 & ELBA CANAHUIRE~

1 Grupo DePSEA, Facultad de Ciencias Biol6gicas. Universidad Nacional Mayor de San Marcos, Apartado 1898, Lima-100, Peru. Alfred-Wegener-Institut fiir Polar- und Meeresforschung, Columbusstrasse, D-27568 Bremerhaven, Germany.

With 8 figures and 2 tables

Key words: El Niiio, benthic community, hypoxia, Humboldt Current.

Abstract. Monthly changes in the community shucture of hypoxic soft-bottom macrobenthos have been studied at a station at 34 m depth in Anc6n Bay (Peru) before and during two El Niiio (EN) events. Of these events, 1982-83 is considered the strongest, and 1991-93 one of the most prolonged in the 20th century. On the oceanographic scale, EN 1982-83 ranges as "very strong", whereas EN 1991-93 ranges as "moderate".

The thermal anomalies at the station during EN 1982-83 (+ 7.8 "C) were almost twice those of EN 1991-93 (+ 4.1 "C). However, the community changes were not in all cases proportional to the extent of warming. Species numbers increased in a similar way (up to 24 species from near zero in each of the two events), but maximum faunal density was five times higher, and mean biomass was twice as high in 1982-83 compared with the event a decade later. Species diversity was slightly higher during EN 1982-83, whereas successional and trophic changes occurred on a broader scale during EN 1991-93. On the whole, the impact of the long-lasting event on the small soft-bottom macrofauna was not much weaker than that of the exceptionally strong event.

The authors discuss the mechanisms which may be responsible for the differences and similarities encountered in the benthic community dynamics during these two events. Both in the unusually strong and the unusually long EN, the community revealed a pattern of early biological response several months ahead of the onset of local warming which marks the official begin of EN. The question is addressed to what extent the increase of certain parameters in the benthic community could be used for predictive purposes.

Problem

There are many indications that the effects of El Niiio-Southern Oscillation (ENSO) are of global dimensions (GLANTZ et al., 1987; GLYNN, 1989; AW & FAHRBACH, 1991). However, El Niiio, the oceanographic component of ENSO, continues to affect most strongly the countries on the South American Pacific coast exposed to the Humboldt Current, with both ecological and economic consequences of great

U. S. Copyright Clearance Center Code Statement: 0173-9565/96/1701 - 0425 $ 11.50/0

426 TARAZONA, A m & CANAHUIRE

magnitude (BARBER & CHAVEZ, 1983; ARNTZ, 1986; PAULY et al., 1987, 1989; GLYNN, 1988,1989; IOC, 1989; ARNTZ & TARAZONA, 1990a).

An El Niiio event may last between a few months and several years. Its strength varies along a scale from weak through moderate and strong to very strong (QUINN et al., 1987). By far the strongest event this century, and the best documented, was that of 1982-83 (for a compilation of the effects and the literature see ARNTZ & FAHRBACH, 1991). It caused all those damages to fisheries and the marine ecosystem that had been reported from former strong events, such as disappearance of shoaling fish, breakdown of food webs, and mass mortalities of invertebrates and warm-blooded animals. At the same time, however, it became clear that there were also many positive effects due to increased oxygenation of the otherwise hypoxic seafloors, reduced predation and grazing in the intertidal, immigration from tropical zones, and competitive advantages of those species whose ancestors formerly inhabited warmer waters ( A m , 1984, 1986; TAWONA, 1984; WOLFF, 1987; ARNE et al., 1988). One of the most striking positive developments was that of macrozoobenthos living on shallow hypoxic bottoms off the Peruvian central coast (TARAZONA et al., 1988 a,b; TARAZONA, 1990).

El Niiio (EN) effects tend to decrease with distance from the equator. The same species may suffer from disastrous EN effects close to the equator and thrive well some 20-30 degrees of latitude further south (ARNTZ & TARAZONA, 1990b). We are far from a full understanding of the mechanisms involved in the changes caused by EN, despite a greatly improved knowledge of benthic communities as compared with the situation one or two decades ago ( A m et al., 1991). We hypothesize, however, that many of the effects that were observed during and after EN 1982-83 occur only during very strong events, whereas such consequences be absent, or change greatly, during moderate and weak events, thus resembling rather the situation at higher latitudes during strong EN.

Since 1983, two moderate El Niiios have occurred. Some material is available from 'the 1986-87 EN, but it has not been fully worked up. On the other hand, data are available from EN 1991-93, which was of similar strength as EN 1986-87, but turned out to be one of the most prolonged events this century*.

Its remarkable advances and retreats caused a discussion among the physical oceanographers on whether it had to be considered as a single or several successive events. For the North Pacific it has even been suggested that the prolonged nature of the recent event may be a consequence of EN 1982-83 (JACOBS et al., 1994; MCPHADEN, 1994).

For biological purposes, this is of minor importance. The question rather is, has a moderate event of long duration (1991-93) a similar or a basically different impact on the shallow benthic ecosystem of the Humboldt Current if compared to a very strong EN (1982-83)? Also can the responses of some of the species, or of the benthic community as a whole, be used as biological indicators for the presence of EN, even though from the oceanographic data the situation may not at all be clear? For this purpose we will analyze recent data from a shallow-water station in the Bay of Ancbn, central Peru, and compare them with data from a previous event.

* There are indications that it is still continuing now (March 19951, and may even have strengthened.

Impact of "El Niiio" on soft bottom macrobenthos 427

Material and Methods Samples for this study were taken from a fixed station at 34 m depth in Anc6n Bay, Peru (1 1'46' S, 77' 12' W), between September 1981 and September 1984, and between March 1990 and December 1993. Macrombenthos was sampled monthly using a 0.04 m2 VAN VEEN grab lowered by hand. At each date, 5-7 samples were taken, of which 3-5 samples were analyzed for their faunal content. Near-bottom temperature and dissolved oxygen concentration were determined from water obtained with a Niskin bottle, equipped with inverted thermometres, from approximately 0.5 m above the seafloor.

Sea-surface temperatures (SST) were used from Isla La Vieja, Independencia Bay, where there is a daily registration at 1390 hours. These values do not differ substantially from those of Anc6n Bay (TARAZONA er al., 1991). Occasionally some additional subsamples were taken for granulometric analyses and to measure the organic content of the sediment.

Each sample was washed on a screen of 0.5 mm mesh size. The material retained by the sieve was transferred to plastic jars and fixed with 7% formalin-seawater. In the laboratory the fauna was separated and identified to species where this was possible. Since the giant filamentous bacteria (Thioploca) could not be counted, their abundance was considered 1 when they were present in a sample; however,the bacteria were weighed. Large nematodes retained by the sieve were counted and weighed as macrofauna.

Wet weight was obtained after putting the fauna shortly on blotting paper, weighed with a precision better than I%, and later transformed into ash-free dry weight (AFDW) using conversion factors which had formerly been determined for each species (TARAZONA et al., 1988 b). Oxygen concentration was measured in the laboratory using standard methods (STRICKLAND & PARSONS, 1968).

H' diversity was calculated as taxonomic diversity, i.e., separating species wherever possible and taking the remaining higher categories as 1 species, from the abundance data. We used the formula of SHANNON-WIENER derived from information theory (SHANNON & WEAVER, 1949). applying log2. In this paper only the H' values have been plotted, since hardly any additional information was contributed by the evenness (J') figures, which were also calculated.

The benthic fauna was grouped into 4 different trophic categories: suspension feeders, deposit feeders, carnivores, and scavengers (see Table I ) . For certain purposes the two latter groups were combined (Table 2). A fifth trophic category (chemoautotrophs) is represented by the giant sulfur bacterium Thioploca.

The levels of significance for the comparisons between the 3 periods before, during, and after EN of each of the community parameters were determined with a one-way analysis of variance and a multiple comparison test, in some cases also using the KRUSKAL-WALUS test (SACHS, 1978).

For the analyses of classification and ordination, a similarity matrix was prepared based on the samples from the different sampling dates. We applied the BRAY-CURTIS index to data previously transformed to log (I+x). Non-metric multidimensional scaling (NMDS) was used as a technique for ordination (FASHAM, 1977; PRENTICE, 1977), and the unweighted pair group method using arithmetric averages (UPGMA) was used as a classification technique (SNEATH & SOKAL, 1973).

Results 1. Temperature and oxygen

Sea-surface temperatures (SST) reveal that warming above the long-term pattern in shallow waters of the Peruvian central coast began from the end of June 199 1 (Fig. 1, above). We assume this to be the real onset of EN 1991-93, although there was another slight temperature decline in late winter 1991. The "official" onset of this EN was fixed for the second half of December 1991 (ERFEN, 1992).

To account for this problem, our figures always mark both dates, the start of EN in June suggested by us, and the "official" onset towards the end of 1991. The first warming off Peru lasted until late May 1992, reaching peak anomalies in March. After a break, warming started again in the 1993 southern hemisphere summer and lasted until August 1993. EN 1991-93 thus had a total duration of about 25 months if we assume its start in June 199 1. Close to the seafloor the temperatures show a similar pattern (Fig. 1, centre); however, it is evident that the winter low was strongly reduced in 1991. Peak anomalies in March 1992 were + 4.1 "C in near-bottom waters.

428 TARAZONA, A m & CANAHURE

Table 1. Species composition at 34 m depth in Anc6n Bay, Peru, before, during, and after the 1982-83 and 1991-93 El Nifio. B - before El Niiio, September 1981 to September 1982; March 1990 to June 1991 D - during El Niito, September 1982 to July 1983. July 1991 to August 1993 A1 - after El Niiio, August 1983 to May 1984; September 1993 to December 1993 A2 - after El Nifio, June 1984 to September 1984

EN 1982-83 EN 1991-93 B D A1 A2 B D A1

MOUVSCA Bivalvia indet. (SU) I * * Bulls sp. (CA) I * * Cwningia murica SOWERBY, 1833 (SU) 0 Gasrropoda indet. (SU) I *

*

Mysella sp. (SU) I * * Nassarius dent@ (POWYS, 1835) (SC) 0 * * * * Nassarius sp. (juvenile) (SC) 0 * * * Pirar catharius (DALL, 1902) (SU) 0 Polinices uber (VALENCIENNES, 1832) (CA) 0

* *

CRVSTACEA Amphipoda 1 (DE) 0 Amphipoda 2 (DE) 0 Amphipoda 3 (DE) 0 Brachyura 1 (CA) 0 Brachyura 2 (CA) 0 Galarheoidea (CA) 0 Callianassa garthi RETAMAL, 1975 (DE) 0 Lepidopa chilensis LENZ, 1902 (SU) 0 Pagurus sp. (CA) 0 Penaeidae (CA) I Pinnixa sp. (SU) 0 Pinnixa transversalis (SU) 0 (H. MILNE EDWARDS & LUCAS, 1842) Pinnixa valdiviensis RATHBUN, 1907 (SU) 0

* * * * *

* * * * * *

* *

* * * * *

* * *

* * * * *

* *

* *

* * Squilla panamensis BIGELOW, 1891 (CA) I *

POLYCHAETA

*

Amphidurus sp. (CA) 0 *

Arenicola sp. (DE) 0 * Aricidea sp. (DE) 0 * Boccardiapolybranchia (HASWELL, 1885) (DE) 0 * Capitella sp. (DE) 0 * Caraziella carrascoi BLAKE, 1979 (DE) 0 * Chaeroprerus sp. (SU) I *

Chone paracincra (SU) HARTMANN-SCHR~DER, 1962 0 Cossura chilensis (DE) I HARTMANN-SCHR~DER, 1965

Glycera americana LEIDY, 1855 (CA) 0 * * Glycera sp. (CA) 0 *

Hannorhoii brevipalpa (CA) 0 BERGSTROM, 1916 * * Hannorhoii sp. (CA) 0 * * Laonice sp. (DE) I *

Ancisrrosyllis hamara HARTMAN. 1960 (CA) 0 * * *

Chaerozone sp. (DE) R * * * * * *

* Diopatra rhizoicola (SC) 0 HARTMANN-SCHR~DER, 1960 * * *

Gyptis sp. (CA) 0 * *

Impact of "El Niiio" on soft bottom macrobenthos

Table I (continued)

429

Leiroscoloplos chilensis (DE) I (HARTMANN-SCHR~DER, 1965) * * * *

Magelona phyllisae (DE) R JONES, 1963 Lumbrineris rerraura (DE) 0 (SCHMARDA. 1861)

Mediomclsrus branchiferus (DE) 0 HARTMANN-SCHR~DER. 1962 * * Mediomasrus sp. (DE) 0 * *

* * * * * * * *

Minuspio sp. (DE) 0 * * Nephfys oculata (CA) 0 HARTMANN-SCHR~DER, 1959 Nephtys ferruginea HARTMAN, 1940 (CA) I

* * *

Noromartus magnus HARTMAN. 1947 (DE) I Onuphidae indet. (CA) 0 * Ophiodromus sp. (CA) 0 * Orbiniidae indet. (DE) 0 * Owenia collaris HARTMAN, 1955 ( S U ) 0 * *

*

Parandalia fauveli (CA) R (BERKELEY & BERKELEY. 1941) Paraprionospio pinnafa (DE) 0 (EHLERS, 1901) * * * * * *

* * * * * *

Pectinaria sp. (DE) 0 * * * * Pholoides tuberculata (CA) 0 HARTMANN-SCHR~DER, 1965 * * * * Polydora sp. 2 (DE) 0 Polydora sp. 4 (DE) 0 Polynoidae indet. (CA) I

* * *

Prionospio (A,) peruana (DE) 0 (HARTMANN-SCHR~DER, 1962) Prionospio sp. (DE) 0 Pseudopolydora sp. (DE) I Sabellaria nanella ( S U ) I CHAMBERLIN, 1919 Sigambra bassi (CA) R (HARTMAN, 1947) Spiochaetoprerus sp. (DE) 0 Spiophanes bombyx (DE) 0 (CLAPAREDE, 1870) Spiophanes soederstroemi (DE) 0 HARTMAN, 1953 Sfhenelais koepckei (CA) 0 HARTMANN-SCHR~DER. 1960 Tharyx aequisefa (DE) 0 HARTMANN-SCHR~DER, 1962

* *

* *

* * * * * * * * * *

*

* *

* * *

Typosyllis variegata (CA) 0 (GRUBE, 1860) * * * OTHERS

Acfiniaria sp. I (CA) 0 Hemichordafa sp. 1 (SU) 0 Nemaroda (DE) R Nemerrea (CA) 0 Ophiacris kroyeri LOTKEN, 1856 (DE) 0 Ophiuroidea indet. (DE) 0 Phoronis sp. (SU) 0 Thioploca spp. (CH) 0

* * * * * * * * *

* * * * * * * * * * * * * * * *

* * * *

* * * Turbellaria indet. (CA) 0 * *

CH - chemical autotroph; SU - suspension feeder; CA -carnivore; SC - scavenger; DE-deposit feeder; I - immigrant; R - tolerant resident; 0 -opportunist

Warm conditions during EN 1982-83 (Fig. 1 , below) had lasted only 10 months, from October 1982 to August 1983, yet had induced positive anomalies up to + 7.4 "C off Anc6n in June 1983. The 14 "C isotherm reached a maximum depth of 185 m outside the Bay in April 1983 (TARAZONA et al., 1991).

The dissolved oxygen concentration close to the seafloor, which after an irregular increase in June 1990 had been reduced to very low values in November 1990,

near

-bot

tom

tem

pera

ture

[ OC ]

e

sea

surfa

ce te

mpe

ratu

re [ OC ]

Impact of "El NiAo" on soft bottom macrobenthos 43 1

Fig. 2. Dissolved oxygen concentrations close to the seafloor at the 34-m station in Ancdn Bay before, during, and after EN 1991-93 and EN 1982-83. - Shaded area and broken vertical line as in Fig. 1.

increased considerably from June 1991, reached a peak of 2.2 ml - 1-1 in December, and remained above 1 ml .1-' until August 1992 (Fig. 2, above). In January 1993, oxygen concentrations were very low, but during the following months there was another increment, with values persisting above 0.5 ml . I-' . EN 1982-83 had revealed a similar pattern, with a strong 0 2 increase starting in July 1982 and high

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sir

4.0

C-N

~sa

riw

dem

fter

5.1

su-P

irur

sp.

10.9

SU

-Pira

r sp

.

13.1

1.

6 SU

-Pho

mni

s sp

.

5.2

SU-P

inni

xa v

aldi

viem

is

3.5

su-o

wm

iaco

unri

r 1.

4 SU

-Pho

roni

r sp.

3.8

DE-

Lrita

rrol

oplo

s ~hi

lrnr

ir

3.4

C-S

igam

bra

bass

i 8.

9 SU

-Pin

niw

mld

ivie

mis

6.

8 D

E-L

r~

sc

olo

~

chile

msu

2.9

SU-P

hom

nirs

p.

5.6

SU-P

irar s

p.

3.6

SU-P

hom

nirs

p.

3.1

DE-

LeM

scol

opbs

chi

lnrr

ir

3.0

DE-

Leiro

scol

oplo

s ch

ilnrr

ic

10.2

DE-

Pecn

Mnh

sp.

0.5

C-S

igam

bm b

assi

1.8

C-G

lyce

m a

me

ric

a~

11.1

SU

-Pila

rsp.

11.0

DE-

L&os

colo

plos

chi

lcnr

is

3.4

3.3 1.8

2.2

1.4

5.2

2.8

2.0

2.8

0.8 2.6

2 ;:;

g 8.

9 0.

1 ?

0.2

5 10

-Jul

-93

C-N

assa

riu

dmti

fcr

91.9

C

-Pam

ndal

ia fa

Uve

li 5.

2 DE

-M-

bmnd

acrv

s 2.

4 D

E-P

arap

rio~

svio

pin~

fa

0.5

DE-

Pect

inar

ia sp

. 0.

1 3

08-A

ug-9

3 C

-Pam

ndal

iafia

uvel

i 85

.0 D

E-Lr

itosc

olop

los c

hilm

rir

5.9

SU-P

inni

w v

nldi

vim

rir

3.1

C-S

igan

abm

bass

i 1.

8 C

H-T

hiop

loca

spp.

1.

2 @

05-S

ep-9

3 C

-Par

Mdo

linfia

uwli

43.3

DE-

Actk

iari

a 31

.1

DE

-Pin

nirn

wld

ivie

nrir

9.4

DE-

LeiIo

scol

oplo

s chi

lens

is 5.

0 C

-Bm

chyu

m 2

2.

6 02

0a-9

3 C

-Bra

chyu

rn 2

71

.0 D

E-Pa

rapr

ioM

spw

pin

fhYt

0 22

.0 C

-Pho

lOid

cS S

p.

1.0

07-N

ov-9

3 C

-Par

anda

lia fn

vvel

i 82

.8 C

-Bra

chyn

rn 2

15

.6 S

U-P

horo

nis s

p.

0.8

DE

Nem

atod

a 0.

1 09

-Dee

-93

C-P

aran

dalia

fauv

eli

91.1

DE-

L.eU

osco

~vlo

s chile

nsis

2.

0 D

E-Pa

rapi

oMsv

io v

im

0.

3

DE - de

posi

~ feed

ers;

C - ca

miv

orcs

& sc

avengers; SU - s

uspe

nsio

n fd

m; CH - T

hiD

proc

a (c

bem

o-au

touo

phic

) i?

Tabl

e 2 b

. Dom

inan

t spe

cies

by

wei

ght (

rank

1-5

) and

troph

ic g

uild

s in

the

perio

d Se

ptem

ber 1

981 t

o Se

ptem

ber 1

984

s 5 @

31

Sam

plin

g da

le

1st r

ank

(%)

2ndr

ank

(96) 3

rdra

nk

(96)

41h

rank

(%

) 5l

hran

k (%

) o=

18-S

ep81

D

E-C

haef

omne

sp

66.7

D

E-O

rbin

iidae

33

.3

P 27

-Oct

-81

DE-

Nem

afod

a 10

0.0

20-N

ov-8

1 D

E-N

emat

oda

100.

0

22-A

pr-8

2 D

E-C

haef

ozon

e sp

. 93

.0 D

E-N

emaf

ada

4.1

DE-

Mag

elon

a ph

yllis

ae

2.3

27-J

ul-8

2 D

E-C

haet

ozon

e sp.

41.1

DE-

vage

lona

phy

lluae

35

.3

DE-

Pam

prio

nosp

io pi

nnuf

a 5.

9 D

E-N

emaf

oda

5.9

DE-

Bocc

ardi

a po

lybr

anch

ia

4.1

25-S

ep82

C

-Nas

sari

us d

enrf

er

71.5

D

EZm

avri

onos

vio

pinn

ufa

9.6

DE-

Ovh

iacf

u kro

yeri

6.

9 C

-Bra

chvu

ra 1

E 29

-Ian

-83

DE-

Para

prio

nosp

io pi

nnur

a 62

.6 C

-Nem

enea

18

.4 C

-Nas

sari

us g

ay;

1.5

C-S

igam

bra bassi

5.1

C-D

iopa

rra

rhiz

oico

la

4.0

a N

20-F

eb-8

3 C

-Dio

pafr

a rhi

zoic

ola

37.2

C-N

emen

ea

25.3

C-P

aran

dalia

fauv

eli

10.8

DE

-Par

apri

onos

piop

ita

6.1

C-B

rach

yura

2

4.6

29-M

ay-8

3 SU

-Hem

icho

rdaf

a 17

.3 S

U-P

inni

xa v

aldi

vien

sis

13.2

C-P

aran

dalia

fauv

eli

6.4

C-N

emen

ea

2.2

DE-

Leifo

scol

oplo

s chi

lens

b 0.

4 02

-Jul

-83

C-N

emen

ea

51 .O

C-P

aran

dalia

fauv

eli

21.2

DE-

Ma8

elon

a ph

yllis

ne

7.0

DE-

Svio

chae

ropt

enu

sp.

6.1

C-S

iRam

bra b

assi

4.

0 13

-Aug

-83

C-N

emer

tea

5 1 .l

C-P

aran

dalia

fauv

eli

30.0

C-S

igam

bra

bass

i 8.

4 D

E-M

agel

ona p

hyllu

ae

3.4

DE-

Para

prio

nosp

io p

imaf

a 3.

3

2

30-D

ec-8

1 D

E-Ch

aero

zone

sp.

62

.8

C-P

holo

ides

sp.

15.6

C-T

ypos

yII~

sp

11.8

DE-

Aric

idea

sp.

7.8

DE

-Nem

odn

2.0 ;

B 26

-Jun

-82

DE-

Pam

prio

nosp

io p

innu

fa

62.6

DE-

Nem

alod

a 37

.5

2.2

3 3.

3 C

-Nem

enea

05

-Dec

-82

DE-

Pam

prio

nosp

io p

innu

fa

61.9

C

-Pam

ndal

ia fa

uvel

i 11

.7 S

U-P

inni

xa fr

anrv

ersa

lu

6.5

C-N

assa

rius

gay

i 5.5

C-N

emen

ea

3.3

i?

17-A

pr-8

3 SU

-Hem

icho

rdar

n 26

.1 C

-Nem

enea

25

.1

SU-P

innr

ro v

aldi

vien

sis

12.8

C-P

amnd

alia

fauv

eli

8.7

C-S

igam

bra bassi

2.8

s

04-S

ep83

02

-&I-

83

30-&

I-83

WD

ec-8

3 15

-Jan

-84

12-F

eb-8

4 04

-Ma-

84

15-A

pr-8

4 12

-May

-84

10-J

un-8

4 22

-Jul

-84

19-A

ug-8

4

DE-

Nof

omas

fus m

agnu

s D

E-Le

ifosc

olop

los c

hile

nsis

SU

-Hem

icho

rdaf

a D

E-U

agel

ona

phyl

lisae

C

-Par

anda

lia fa

uvel

i D

E-Le

ifosc

olop

los c

hile

nsis

C

-Par

anda

lia fa

uvel

i D

E-Le

ifosc

olop

los c

hile

nsis

C

-Par

anda

lia fa

uvel

i D

E-Bo

ccar

dia p

olyb

ranc

hia

DE-

Nem

atod

a SU

-Hem

icho

rdat

a

41.4

DE-

Mag

elon

a ph

yllis

ae

28.4

C-N

emen

ea

41.4

C

-Par

anda

lia fa

uvel

i 50

.0 C

-Par

andn

lia fauveli

11.3

C-S

igam

bm ba

ssi

28.6

C

-Gly

cera

am

eric

ana

61.0

C-N

emen

ea

22.0

C

-Nas

sari

us d

entif

er

82.6

C-N

emen

ea

50.0

DE-

Nem

afod

a

88.6

C-P

oron

dalia

fauv

eli

100.

0

11.6

21

.4

24.1

22

.8

16.1

20

.3

19.1

11

.2

10.4

50

.0

10.5

C-P

aran

dalia

fauv

eli

C-P

aran

dalia

fauv

eli

SU-P

inni

xa fr

ansv

erso

lis

DE-

Leito

scol

oplo

s chi

lens

is

C-N

emen

ea

C-P

aran

dalia

fauw

li

DE-

Mag

elon

a ph

yllis

ae

C-N

emer

fea

DE-

Mag

elon

a ph

yllu

ae

DE-

Mag

elon

a ph

yllis

ae

10.8

DE-

Leifo

scol

oplo

s chi

lens

is

20.5

D

E-No

rom

osru

s mag

nur

1.9

DE-

Para

prio

nosp

io p

if

a

10.0

C-B

mch

yura

2 4.

3 D

E-M

agel

ona

phyl

lisae

11

.0 C

-Nas

sari

us d

entiy

er

1.9

C-S

igam

bm ba

ssi

14.2

C-P

aran

dalia

fauv

eli

3.4

C-S

igam

bra

boss

;

0.7

DE-

Cha

efoz

one s

p.

8.0

DE-

Pse&

poly

dora

sp

.

6.8

DE-

Leifo

scol

oplo

s chi

lens

is

5.4

DE-

Para

prio

nosp

io pi

nnuf

a 3.

1 D

E-C

haef

owne

sp.

9.4

DE-

Thar

yx a

equb

efa

5.8

DE-

Cha

etow

ne sp

. 13

.1 D

E-C

haef

owne

sp.

1.3

C-N

assa

rius

juv.

18.3

DE-

Poly

dora

sp. 2

0.1

DE

-Nem

&a

6.9

3.1

6.4

4.1

1.6

8.3

2.3

8.9

0.9

0.0

22-S

epM

D

E-N

emaf

oda

100.

0

DE - d

epos

it fe

eden

; C -

carn

ivor

es &

scav

enge

rs: S

U - su

spen

sion

feed

ers;

CH - T

hiop

loca

(che

rno-

auto

tmph

ic)

ti w


concentrations lasting more than a year beyond the local warming event. The peak values just before warming started and towards the end of the event (3.8 do2 '1-1) clearly exceeded those of EN 1991-93 (Fig. 2, below).

2. Impact on community structure Species composition before (March 1990 to June 1991), during (July 1991 to August 1993), and after EN 1991-1993 (up to December 1993) can be seen in Table 1. Before EN the maximum number of species in the samples was 9, in July 1990, and the cumulative number of species during the whole period was 13 (Fig. 3, above). During the event the maximum number was 24 (in March 1992), and the cumulative number of species reached 45. The incorporation of "new" species into the community was particularly intense in July 1990, July 199 1, and in January and March 1992 (same Fig.). During the 1982-83 event, the maximum number of species in the samples had also been 24 (in December 1982, two months after the onset of warming); however, the cumulative number of species then was 72 (Fig. 3, below). All the taxa encountered during the different phases of the two events are presented in Table 1, which also distinguishes trophic groups and life strategies (opportunists, immigrants, and tolerant residents).

Taxonomic diversity increased in both events, 1991 and 1982, as early as July (Fig. 4). However, there was also a distinctly higher diversity in July 1990, related to the strong, irregular 0 2 increase that year (cf. Fig. 2). Highest values were calculated for March to July 1992 and February 1983; the 1982-83 values were apparently similar to those of 1991-93.

Before warming occurred, macrobenthos densities were low in 1991, with a maximum of 13.3 indiv. . (0.04 m2)-1 in April (Fig. 5, above). During EN, maximum densities reached 8 times higher values, with 101.7 indiv. . (0.04 m*)-1 in February 1992. During the 1982-83 event, a maximum density of 5 12 indiv. . (0.04 m2)-1 had been recorded in December 1982, two months after the onset of warming.

Total biomass during EN 1991-93 was strongly influenced by filamentous bacteria (Thioploca), which in some months constituted over 99% by weight. Before EN, total biomass was on a low level, with a maximum of 0.0046 g AFDW . (0.04 m2)-' in July 1990. During the event it increased by a factor of 28 and reached a maximum of 0.1268 g . AFDW . (0.04 m2)-1 in September 1991 (Fig. 6, above). Biomass of the macrofauna alone climbed to a maximum of 0.0461 g AFDW . (0.04 m2)-* in March 1992. During EN 1982-83 biomass fluctuations had been similar to those in density, initially without a time lag between the density and biomass peaks, and biomass attained its maximum of 0.276 g AFDW . (0.04 m2)-1 in December 1982 (Fig.6, below).

3. Impact of EN on dominant taxa and trophic structure The dominance of individual taxa (rank 1 to 5 by weight; numbers had to be omitted due to space restrictions by the editors) representing the principal trophic guilds at the different sampling dates during EN 1991-93 is presented in Table 2 a. Before that EN there was an almost total dominance by deposit feeders, principally the polychaetes Paraprionospio and Pectinaria, nematodes, and the ophiuroid Op- hiacris. As early as in April 199 1, the carnivorous polychaete Parandalia and the

Impact of "El NiRo" on soft bottom macrobenthos 435

cn a 0 a P

.-

Fig. 3. Variations in the number of species present at any time, of "new" species joining the community, and of the cumulative species number at the study site before, during, and after EN 1991-93 and EN 1982-83. - Shaded area and broken vertical line as in Fig. 1 .

436 TAJWZONA, A m t CANAHUIRE

Fig. 4. H' taxonomic diversity (cf. "Methods") of macrobenthos (k SE) at the study site before, during, and after EN 1991-93 and EN 1982-83. - Shaded area and broken vertical line as in Fig. 1.

Impact of "El Niiio" on soft bottom macrobenthos

n

n (u

7 I

E

.

437

Fig. 5. Density of macrobenthos (* SE) at the study site before, during, and after EN 1991-93 and EN 1982-83. -Shaded area and broken vertical line as in Fig. 1.

438 TARAZONA, A m & CANAHIJJRE

Fig. 6. Biomass as ash-free dry weight of macrobenthos (p SE) at the study site before, during, and after EN 1991-93 and EN 1982-83. -Shaded area and broken vertical line as in Fig. 1.

Impact of “El Niiio” on soft bottom macrobenthos 439

gastropod Nassarius, a scavenger, took over. During the phase between June and December 199 1, which we include under EN, conditions were very much the same as during the subsequent ”official” EN period, with an overall weight dominance by the filamentous sulfur bacterium Thioploca and numerical dominance of the suspension feeders Owenia (a polychaete) and Phoronis, the camivorous/scavenging polychaetes Parandalia and Sigambra, and continued importance of the deposit feeders Paraprionospio and Pectinaria. Up to the end of EN, however, none of the deposit feeders returned to the 1st rank, although other polychaetes of this group, Leitoscoloplos and Mediomastus, increased in importance. Suspension feeders such as the crab Pinnixa and the bivalve Pitar constituted a larger share both by number and biomass. The situation after the 1991-93 EN cannot be evaluated properly because the period from September to December 1993 is too short; however, deposit feeders seem to return to the first ranks again.

The trophic dynamics of EN 1982-83 can be seen from Table 2 b. Then, too, there was a strong deposit feeder dominance before the event, with the polychaete Chaetozone and nematodes as principal dominants besides the species that have been mentioned for this phase a decade later. During EN proper, almost the same deposit-feeding dominants (plus Chaetozone) were found as during the 1992-83 EN, and there were also most of the same representatives of the carnivore/scavenger group (plus nemerteans and Diopatra, another polychaete). However, suspension feeders were almost absent except for a few Owenia and Pinnixa. Immediately after EN, deposit-feeding polychaetes became very strong, with Paraprionospio, Leito- scoloplos, and Magelona, but subsequently there was again a greater trophic spec- trum which also included Parandalia, Sigambra, and nemerteans. In the final phase, nematodes became the principal dominant again, and the community returned to an impoverished stage as before the event.

Based on Nh4DS ordination techniques and using abundance data of the species in Table 1 for the periods referred to in that table, Fig. 7 reveals for the 1982-83 EN that conditions before and a long time after EN (periods B and A2) were very similar, as were also the conditions during and immediately after the event (D and ’

Al). In the case of EN 1991-93, the dissimilarity between the ongoing event, the samples of which form a distinct group (D), and the other periods is fairly obvious, although conditions after EN (Al) seem to swing back to those before EN (B) already in the final phase of warming, i.e., in July 1993. No data are as yet available for the A2 phase.

The oscillations of the dominant species at the Anc6n Bay station (Fig. 8) reflect the poor state of the community under hypoxic conditions in both periods of observation and the favourable development during EN, i.e., due to oxygenation. There are, however, differences in the shape of the populations after EN which are difficult to relate to the oxygen situation. Most of the populations continue favour- ably for about 11 months after EN 1982-83, but break down either in the later phase or almost immediately after EN 199 1-93.

Discussion

Even more so than those of the 1982-83 EN, the biological data of EN 1991-93 call for a revision of the actual El Niiio definition by SCOR. Off California, there was a first SST increase in June, another increase - related with positive sea-level anom-


alies - in September 1991, but a steady increase of SSTs (and thus the "official" begin of EN in that area) was noticeable only from January 1992 (HAYWARD, 1993). The physical oceanographers maintain that off Peru, EN 1991-93 commenced in late December 1991 (ERFEN, 1992). Our biological data suggest, however, a persistent increase of all community parameters as early as late June 1991. The biologists would be happy to accept this as an indication of the higher sensitivity of the benthic fauna (or, in other cases, of certain planktonic or fish indicator species; cf. CPPS, 1993) as compared with oceanographic equipment. On the other hand, a closer look at the oxygen data (see Fig. 2) renders it most likely that it is precisely the increase of oxygen that stimulates benthic immigration, colonisation, and development. The major deficiency of the SCOR definition may be its exclusive fixation on sea surface temperatures (SSTs), a parameter which presents a distinct increase, beyond the normal seasonal oscillations, only when major Kelvin waves arrive at the South American continent. At this time, however, biological change had been under way for quite some time in each of the two ENS considered in this paper.

It might thus be preferable to base a timely decision on whether there another EN is approaching on the oxygen increase at the seafloor rather than on SSTs. Our problems in attempting to do so lie in the irregular oxygen increases, which at first glance cannot be distinguished from the more persistent (although strongly oscillat- ing) oxygenations that are typical of EN. Even smaller increases of dissolved oxygen, e.g., that of July 1990, cause an immediate increase in species number, H' diversity, and - to a lesser degree - in density. There are insufficient data from, between-EN periods at this time to determine whether irregular 0 2 increases during non-EN conditions are a common pattern in shallow water off Anc6n. or whether they are recent, representing another long-lasting effect of the great 1982-83 EN (MCPHADEN, 1994). Perhaps the parameter "benthic density" could be helpful in recognizing EN at an early stage: if densities remain low, despite the Occurrence of an oxygen peak, there is no Nifio yet. H' diversity-and species numbers seem to be too sensitive, and biomass too slow to fulfil this task.

For the time being the shaded areas in the graphs reflect the official version of the onset of EN 1991-93, but it is obvious that in doing so, major developments in the benthal, both physical and biological, are out of scope. We suggest that both the oxygenations between June and December 1991 and the strong changes in the faunal parameters during this period have to be related to El Nifio. The NMDS similarity data of Fig. 7 clearly support this view.

During EN 1982-83, both the highest temperature anomalies and the highest oxygen concentrations were almost twice as high as the corresponding values during EN 1991-93. This greater strength should imply major changes in the displacement of water masses, the deepening of the thermocline, and advection of larvae (TARAZONA et al., 1988a; ARNTZ & TARAZONA, 1990b; A m & FAHRBACH, 1991). Advection and immigration of "foreign" species and colonization from neighbouring areas, as represented by the cumulative species number, were in fact much higher during EN 1982-83 (72 vs. 45 species). The number of species joining the community at the moment of maximum immigration was nearly 3 times higher during the strong EN compared with the long-lasting event (16 vs. 6). However, the maximum number of species recorded simultaneously during either of the two events was the same (24). Two degrees of latitude further south, in Independencia Bay, a highly productive area of about the same depth and similar sediment


..---- c - *

SEP.4 , $ ' I I I I

B .' , t 'A2

, . .I (stress coeftkient 0.096)

NMDS I

D

NMDS I Fig. 7. Non-metric multidimensional scaling ordination based on the similarities of the abundance data of macrobenthic species at the study site before (B). during (D), shortly after (Al), and long after (A2) EN 1982-83 and before, during, and shortly after EN 1991-93. Arrows indicate succession of major changes in time.

442 TARAZONA, ARNTZ & C A N A H ~ R E

conditions, but favoured by better oxygenation, 36 macrobenthic species were recorded together under non-EN conditions (TARAZONA, unpubl. data). Thus, nei- ther a very strong nor a very prolonged EN event produce conditions in our hypoxic area of study which may be considered normal, despite significant increases in the species number. With regard to the pattern of recolonisation (not its intensity!), a long duration EN impact does not differ much from a very strong EN impact.

Why does the ecosystem not recover to a higher level of species richness during EN? Obviously, even a very prolonged event does not last long enough to allow for the development of many species that appear late in succession, have a long life span, or are sensitive to frequent oxygen reductions, as is demonstrated by the scarceness of echinoderms, molluscs, and large crustaceans off Anc6n. PEARSON & ROSENBERG (1987) have predicted a suite of small, opportunistic species for such physically unstable areas. Furthermore, the oxygen increase related to EN is not continuous but rather occurs in pulses (TARAZONA et al., 1991), possibly following largely the pulses of intermittent waves which are propagated along the coast (BOHLE-CARBONELL, 1989).

Maximum densities during the strong EN 1982-83 were five times those of the prolonged EN 1991-93, whereas biomass was only twice as high in the former event. In the initial phase of EN 1991-93, there was a time lag between the peak densities and the peak biomasses, which was not registered during the 1982-83 event. This is consistent with the finding that a much profounder change of trophic function occurred in the recent EN.

Examining the dominance of trophic groups and individual species, the two EN differ considerably, although most principal actors are among the same, about 20, taxa (see Table 2). Exceptions among the species of major significance were Chaetozone sp. and Nassarius dentifer, which were common only during EN 1982-83, and Owenia collaris and Pitar catarius, which held dominant positions only during EN 1991-93.

The period before EN is characterized in either case by an overwhelming dominance of deposit feeders both by number and biomass, as would be predicted for an area with low water exchange where sedimentation rates are high (PEARSON & ROSENBERG, 1987). During EN this predominance is weakened (as occurred during the strong event) or reversed (during the long event), and representatives of the carnivordscavenger group or the suspension feeders and even the chemo-autotro- phic bacteria (the latter two only during EN 1991-93) may take over. Actually, the deposit feeders do not at all disappear during the presence of EN; on the contrary, many of them even increase notably (see Fig. 8), but most of the time they lose their dominant position. The long-lasting dominance of filamentous bacteria (Thioploca) during the 1991-93 EN was quite a surprise for us since we assumed that these organisms would not be serious competitors for macrobenthos under greatly improved 0 2 conditions (ARNTZ et al., 1991). The shifts of individual species within the various trophic groups are quite complex and may well reflect particular reproductive events ("clouds" of recently released larvae) within the process of succession.

The phase after EN can at this time only be evaluated for the 1982-83 EN since the results from the long-lasting event are not yet available. In 1983 the deposit feeders became dominant again quite rapidly, but the other trophic groups continued to have important shares. One year after the end of the anomalies the community had not yet completely returned to its pre-EN stage.

Impact of “El Nifio” on soft bottom macrobenthos 443

Fig. 8. Fluctuations of dominant macrobenthic species at the study site before, during and after EN 1982-83 and EN 1991-93. Values are densities per 0.04 m2 transformed to log (l+n). Chaerozone and Nassurius were dominant only during EN 1982-83, Oweniu and Piruronly during EN 1991-93. - Shaded area and broken vertical line as in Fig. I .


Summarizing the trophic changes at the 34-m station off Ancbn, the long EN involved much more notable shifts than the strong EN. This would not be so surprising if these changes had not started directly at the beginning of the event or even - accepting the "official" onset of EN 1991-93 - several months before. This is another indication that our starting date represents the onset of EN better than the official date. Apparently, beyond the strength of physical change during EN, the exact timing of the event is even more important for the availability of larval colonizers than we thought hitherto (ARNTZ, 1986; ARNTZ et al., 1988).

Considering life strategies, the overwhelming majority of the colonizers are opportunists which react quickly to improved 0 2 conditions. Also the "tolerant residents" (TARAZONA et al., 1988b) such as nematodes, filamentous bacteria, and certain polychaetes have strong opportunistic traits. The group of immigrants (e.g., Leitoscoloplos, Noromstus, Subellaria) plays a very minor role at this station, which is characterized by small macrobenthos, compared with, e.g., the motile megafauna in other areas of the Humboldt Current (ARN'IZ & FAHRBACH, 1991). Most changes in the Anc6n Bay community are due to the development of autoch- thonous species living in better flushed areas close by, for example in even shal- lower areas, or in small, disperse populations in the oxygen minimum zone.

All dominant species fluctuate intensely (cf. Fig. 8), mostly in connection with the changing oxygen situation. There was an early increase of many species during the two ENS which might be of future predictive value. The differences between the two events in this respect can be related to the seasonal availability of reproductive stages, but also to the fact that the "official" onset date of EN 1991-93 may not correspond to reality. On the other hand, the state of the populations after EN may indeed reflect differing effects of a very strong and a long-lasting event. At least for the shallow-water, soft-bottom benthos, however, the data at hand do not support our initial hypothesis that a moderate, though extended, EN event has a much weaker impact on the fauna than a very strong one.

Summary

The comparison of the biological effects caused by a very strong El Niiio (1 982-83) and the recent, very long but moderate event (1991-93) on a normally hypoxic, macrobenthic, soft-bottom community off Peru reveals certain differences, but the overall pattern of change was found to be similar. The most important factor of change in both cases was oxygenation which occurred in pulses and began before the official onset of EN, which is determined by a steady temperature increase. All dominant species, most of which are opportunists, fluctuate intensely with the changing oxygen situation. Under "strong EN" conditions, densities and biomasses climbed to five- and two-times higher peaks, respectively, compared to the "long EN", but species numbers increased in a similar way. Trophic changes were more marked during the recent, extended event.

Acknowledgements

The authors would like to thank the editors for their great patience with the delivery of the manuscript, and an unknown referee for his useful comments. CLAUDIA PICHLER-DIECKMANN invested much effort


in the improvement of the original graphs, and MANUELA CH~OUI-ROMBOY also improved the tables and corrected several versions of the text.

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Documents

Impact of Two “El Niño” Events of Different Intensity on the Hypoxic Soft Bottom Macrobenthos off the Central Peruvian wast