PLEASE SCROLL DOWN FOR ARTICLE

This article was downloaded by:On: 16 November 2010Access details: Access Details: Free AccessPublisher Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

African Journal of Marine SciencePublication details, including instructions for authors and subscription information:http://www.informaworld.com/smpp/title~content=t911470580

A review and tests of hypotheses about causes of the KwaZulu-Natalsardine runP. Fréona; J. C. Coetzeeb; C. D. van der Lingenbc; A. D. Connelld; S. H. O'Donoghuee; M. J. Robertsf; H.Demarcqa; C. G. Attwoodc; S. J. Lamberthbd; L. Hutchingscf

a IRD, Sète, France b Branch Fisheries, Department of Agriculture, Forestry and Fisheries, Rogge Bay,South Africa c Marine Research Institute, University of Cape Town, Rondebosch, South Africa d SouthAfrican Institute for Aquatic Biodiversity, Grahamstown, South Africa e School of Biological andConservation Sciences, Westville Campus, University of KwaZulu-Natal, Durban, South Africa f

Oceans and Coasts, Department of Environmental Affairs, Rogge Bay, South Africa

Online publication date: 08 November 2010

To cite this Article Fréon, P. , Coetzee, J. C. , van der Lingen, C. D. , Connell, A. D. , O'Donoghue, S. H. , Roberts, M. J. ,Demarcq, H. , Attwood, C. G. , Lamberth, S. J. and Hutchings, L.(2010) 'A review and tests of hypotheses about causes ofthe KwaZulu-Natal sardine run', African Journal of Marine Science, 32: 2, 449 — 479To link to this Article: DOI: 10.2989/1814232X.2010.519451URL: http://dx.doi.org/10.2989/1814232X.2010.519451

Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf

This article may be used for research, teaching and private study purposes. Any substantial orsystematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply ordistribution in any form to anyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss,actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directlyor indirectly in connection with or arising out of the use of this material.

African Journal of Marine Science 2010, 32(2): 449–479

Printed in South Africa — All rights reserved

Copyright © NISC (Pty) Ltd

AFRICAN JOURNAL OFMARINE SCIENCE

ISSN 1814–232X EISSN 1814–2338

doi: 10.2989/1814232X.2010.519451

African Journal of Marine Science is co-published by NISC (Pty) Ltd and Taylor & Francis

A review and tests of hypotheses about causes of the KwaZulu-Natal sardine run

P Fréon1*, JC Coetzee2, CD van der Lingen2,3, AD Connell4, SH O’Donoghue5, MJ Roberts6, H Demarcq1, CG Attwood3,

SJ Lamberth2,4 and L Hutchings3,6

1 IRD, UMR 212 EME, CRHMT, avenue Jean Monnet, 34209, Sète, France2 Branch Fisheries, Department of Agriculture, Forestry and Fisheries, Private Bag X2, Rogge Bay 8012, South Africa3 Marine Research Institute, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa4 South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown 6140, South Africa5 School of Biological and Conservation Sciences, Westville Campus, University of KwaZulu-Natal, Private Bag X54001,

Durban 4000, South Africa6 Oceans and Coasts, Department of Environmental Affairs, Private Bag X2, Rogge Bay 8012, South Africa

* Corresponding author, e-mail: pfreon@ird.fr

Manuscript received June 2010; accepted August 2010

The term ‘sardine run’ is part of the cultural heritage of the South African nation and refers to a natural

phenomenon that is well known to the general public but still poorly understood from an ecologi-

cal perspective. This lack of understanding has stimulated numerous hypotheses, often contradic-

tory, that try to explain why (ultimate factors) and how (proximate factors) the run occurs. Here, we

provide a new definition of the term sardine run, review the various hypotheses about the run, and

propose ways to test those hypotheses. Where possible, the results of tests that have been conducted

thus far are presented and discussed. Our interpretation of the causes is that the sardine run most

likely corresponds to a seasonal (early austral winter) reproductive migration of a genetically distinct

subpopulation of sardine that moves along the coast from the eastern Agulhas Bank to the coast of

KwaZulu-Natal (KZN) as far as Durban and sometimes beyond, in most years if not in every year. This

eastward migration is constrained close to the coast by the thermal preference of sardine and the

strong and warm offshore Agulhas Current. The run is facilitated by the presence of a band of cooler

coastal water and by the occurrence of Natal Pulses and break-away eddies that enable sardine shoals

to overcome their habitat restrictions. These enabling mechanisms are most important in the area

where the shelf is at its narrowest and feature most prominently off Waterfall Bluff, which has led to the

coining of the ‘Waterfall Bluff gateway hypothesis’. Based on the collection of eggs off the KZN coast,

sardine remain there for several months and their westward, return migration during late winter to

spring is nearly always unnoticeable because it likely occurs at depth as the fish avoid warmer surface

waters. Years in which the sardine run is not detected by coastal observers could reflect either its real

absence due to high water temperatures and/or other hydrographic barriers, or an eastward migration

that is farther offshore and possibly deeper and is enabled by hydrographical anomalies.

Keywords: migration, proximate factors, Sardinops sagax, South Africa, ultimate factors

The term ‘sardine run’ (or ‘KwaZulu-Natal sardine run’)

is part of the cultural heritage of the South African nation

and refers to a well-known natural phenomenon off the

east coast of South Africa. The sardine run has long been

known by the coastal population in that region because of

its economic importance (van der Lingen et al. 2010a), and

over the last few decades has been a topic of much media

attention and become the focus of a growing tourism industry

(Dicken 2010, Myeza et al. 2010). Despite this heightened

interest, the ecological aspects of this phenomenon remain

poorly understood, as evidenced by numerous hypotheses,

often contradictory, that try to explain why and how the

sardine run occurs. In this paper, we first attempt to provide

a neutral and consensual meaning of the term sardine run

as perceived by the general public and scientists alike.

Because of the commercial/recreational/public nature of

the sardine run, which requires some kind of management

response that will depend on how accurately the timing

and intensity of the ‘run’ can be predicted, our description

of what constitutes the run focuses on its visible aspects

Introduction

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings450

when it reaches the coast and elicits a human reaction. The

ecological meaning of the sardine run and its management

implications are separate issues that are also addressed in

this paper.

We define the term sardine run as the visible effects of the

coastal, alongshore movement during early austral winter of

a small and variable fraction of the South African population

of sardine Sardinops sagax from the eastern Agulhas Bank

to the KwaZulu-Natal (KZN) coast, as far as Durban and the

north coast of KZN. The sardine run is usually associated

with foraging top predators including seabirds, mammals

(O’Donoghue et al. 2010a, 2010b), and sharks and gamefish

(Dudley and Cliff 2010, Fennessy et al. 2010) that facilitate

its visual detection. The north-east displacement is usually

initiated from late May to early June and is mostly visually

detected and commercially exploited (via beach-seine

netting and tourism operations) when it occurs within a few

hundred metres of the coast. The duration of this coastal

spectacle is highly variable, lasting until the end of June or

even September at times (O’Donoghue et al. 2010c). Little is

known about farther offshore movements of sardine and even

less about the likely return of surviving fish to the Agulhas

Bank thereafter, although eggs in plankton samples suggest

that sardine remain in KZN waters until as late as December

(Connell 2010). Consequently, it is unknown whether or not

the sardine run corresponds to a conventional seasonal

migration that occurs every year but is only partly visible

in some years. Similarly, it is uncertain whether or not the

individuals that perform the sardine run belong to a different

population or subpopulation of sardine from those that inhabit

the west and south coasts of South Africa. Furthermore,

questions regarding the reasons for the variable occurrence,

intensity and duration of the sardine run at different spatial

and temporal scales are still unanswered.

Several hypotheses have been proposed to explain why

and how the sardine run occurs. In this paper, we describe

these hypotheses and examine them in the light of evidence

in the literature, including papers presented in this suite, and

either reject the hypothesis or suggest future research that

might yield further evidence to support a particular hypoth-

esis. General concepts of spatial behaviour that make

a distinction between ‘proximate’ and ‘ultimate’ factors

motivating this behaviour are first presented, followed

by the methods specific to this study and, where relevant,

summaries of those employed in preceding papers of the

suite (van der Lingen et al. 2010b). Hypotheses related to

ultimate and proximate factors of the sardine run and their

corresponding tests, some of which are relevant to more

than one hypothesis, are then detailed. Results of the tests

performed are presented and summarised, followed by a

general discussion that provides insight gathered from these

analyses, and contributes to our present understanding of

the sardine run.

General concepts of spatial behaviour

Proximate versus ultimate factors

Our investigation into the causes of the sardine run is

set against a conceptual framework of animal movement

behaviour and its ultimate and proximate causes. Following

Tinbergen (1963), Noakes (1992) applied the general

terms ‘ultimate’ and ‘proximate’ to refer to different factors

influencing behaviour. Ultimate refers to the final, long-term,

evolutionary consequences of behaviour (function), whereas

proximate refers to the immediate, short-term, physiological

mechanisms of behaviour (causation). Instantaneous habitat

selection is related to proximate cues and is expected to

occur on a small spatial scale (microhabitat) in response

to changes in the environment. A common example of a

proximate factor, likely relevant to the sardine run, is the

avoidance of warm waters and associated oxygen depletion.

This instantaneous selection and its relationship with the

environment are usually easy to observe and quantify. In

contrast, ultimate relationships may be much more difficult to

resolve. Additionally, once a selective pressure has led to the

evolution of a particular behaviour, that behaviour may last

for epochs even when major change occurs in the environ-

ment, providing that the behaviour (termed relic behaviour)

has at most a minimal cost regarding survival and reproduc-

tive success. Examples of ultimate factors are availability of

appropriate food, low potential predation (not instantaneous

predator avoidance) or favourable conditions for reproduc-

tive success.

An understanding of ultimate causes should also provide

insight into the long-term effects of fishing on movement

behaviour. Modern fishing practices have massive eco logical

influences that can impose strong selection differentials (Law

2007). Of particular relevance to this review are studies of fish

that display inter- and intra-population variability in movement

behaviour. The contributions of conditional (environmental)

and unconditional (inherited) factors to this variation is

important. These contributions will be enhanced if the

conditional variation is density-dependant or if the uncondi-

tional variants are exposed to differential fishing mortality

(Attwood and Cowley 2005, Dawson et al. 2006), as is likely

the case for the sardine run.

Types of movement

Although mechanisms of movement may differ, the selection

pressures experienced by aquatic and terrestrial species

are not dissimilar. Classification schemes and definitions

of movement are numerous, and scientists studying fish

movement frequently refer to, among others, residency, natal

homing, nomadism, dispersal, migration and emigration,

although some of these terms are applied loosely and often

not consistently. When considering movement rules for

individual-based models of fish, Tyler and Rose (1994) drew

a distinction between pattern-matching rules and process-

matching rules. Apart from the patterns, the theoretical and

evolutionary models that underpin each type of behaviour

need to be considered.

Some classifications have been based on physical descrip-

tions of the movement (e.g. distance, consistency in

direction, repetition, etc.), whereas others have been based

on biological events (e.g. feeding, spawning, home-range

relocation, etc.). The classification scheme presented by

Dingle (1996) draws on studies across the animal kingdom,

and provides a useful reference (Table 1). Station-keeping

is a widely adopted strategy, even among fish (e.g. Gerkin

1959), but is not likely to apply to sardine. It is the distinc-

tion between ranging and migration that is of relevance to the

current investigation. Ranging (Dingle 1996), or nomadism

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 451

(Sinclair 1984), is a movement pattern that results from

a search for suitable resources and perhaps for a new

home-range. Animals searching for new resources cease

moving once these resources have been located. Definitions

of the home-range are not always practical and include

the following: the area in which an animal normally lives

(Smith 1980); the area that an animal occupies exclusive of

long-range migrations and erratic wanderings (Mace et al.

1984); a specific area that is repeatedly used in the course

of an animal’s activities; and a relatively circumscribed

area over which an organism travels to acquire resources it

needs for survival and reproduction (Dingle 1996). Under the

umbrella of the optimal foraging theory, the marginal value

theorem states that an animal will remain in a particular

location (patch) until the rate of energy gain falls below the

rate achievable elsewhere (Charnov 1976).

Sinclair (1984) uses three terms to describe one-way

movements: emigration, by which the animal moves along

a predetermined direction; dispersal, by which the animal

moves in an unpredictable direction; and nomadism, by

which the animal moves with no consistent direction. Harden

Jones (1968) draws a similarity between wanderings and

dispersal, both of which describe widespread movements of

fish away from the breeding area in search of food. Shields

(1984) defines dispersal as the movement of an animal away

from their site of origin to a new area, or succession of areas.

Dingle’s (1996) ranging is perhaps similar to Sinclair’s (1984)

nomadism and Shields’ (1984) dispersal, but Dingle (1996)

notes that there will remain confusion between foraging and

ranging and between ranging and migration, largely because

specific distinctions have not been looked for.

Migration is typically viewed as a regular round-trip within

the lifespan of an animal (Sinclair 1984), with the basic

plan of a fish’s migration usually being a triangle (Harden

Jones 1968). The free-floating egg is spawned at point A,

whereupon it drifts with the current and develops into a larval

stage. The larval stage reaches a nursery ground, B, where

it develops into a juvenile fish that ultimately recruits to the

feeding ground, C. The adult fish migrates from C to A to

spawn, an act that it may do once only, as is the case for

eels, or repeatedly, over several years, as is the case for

plaice. The most favoured explanation for such a pattern is

that the spawning ground must be upstream of a favourable

nursery ground, hence adults must undertake a compen-

satory upstream migration. The definition of migration may

be broadened and defined as a syndrome that involves

behavioural, anatomical and physiological adaptations.

Harden Jones (1968), for example, defines migration as

‘the class of movement which impels the migrants to return

to the region from where they have migrated’. According to

Dingle (1996), migration should not be defined in terms of

the movement, but rather in terms of the mover. He adopts

a modification of Kennedy’s (1985) definition: ‘Migratory

behaviour is persistent and straightened-out movement

effected by the animal’s own locomotory exertions or by

its active embarkation on a vehicle. It depends on some

temporary inhibition of station-keeping responses, but

promotes their eventual disinhibition and recurrence’. Accord-

ing to this definition, migration involves five attributes that

distinguish it from other movement types (Dingle 1996):

the animal displays persistent motion that takes it beyond 1.

the home-range;

the movement is direct, and not erratic in direction;2.

the animal passes suitable resources that would otherwise 3.

not be overlooked;

the animal engages in specific departure and arrival 4.

behaviour; and

physiological adjustments are made to reserve energy for 5.

a long journey.

Migrants commonly depart before existing resources are

depleted, and, ultimately, migration places the animal (or its

offspring) among favourable resources, thus avoiding the

possibility of it being marooned in a degrading environment

with insufficient resources. Distinctions have been made

between alimental, climatic and gametic migration (Harden

Jones 1968). Often associated with gametic migration is the

phenomenon of natal homing (Carr 1967), made famous by

salmon, the eel Anguilla and turtles, but known to occur also

among truly pelagic fish (Cury 1994, Rooker et al. 2008).

These definitions generate testable hypotheses that we

apply to the sardine run.

Mixed strategies

A difference in behavioural patterns among individuals

within a population is not an anomalous situation, but rather

it might be an evolutionary stable strategy that maintains

a balance between station-keepers and colonisers. At the

root of the split is density dependence. Crowded popula-

tions near or over carrying capacity may respond with

ranging behaviour gaining ascendancy over station-keeping,

implying also that movements at the extreme of the range

are linked to resource limitation within the population. An

example of this is detailed below under the basin theory

hypothesis (MacCall 1990).

Mixed behavioural strategies are common within species

and populations (Swingland 1984) and can easily confuse

the study of fish movement. Movement behaviour is rarely

consistent throughout a species, because most species

Movement type Characteristics

Station-keeping

Kinesis

Foraging

Commuting

Territoriality

Ranging (= nomadism, or = dispersal)

Migration (= emigration + immigration, or = one-way emigration)

Movements that serve to keep an animal stationary

Feeding movements within a home-range

Diel movements between day and night locations

Territorial defence and aggression, non-overlapping home-ranges

Exploratory movements over wide areas in search of resources

Persistent, directed, non-exploratory, predictable, physiological adaptation

Table 1: Dingle’s (1996) classification of animal movement behaviour, with synonyms inserted in brackets

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings452

show qualitative (i.e. type of movement) and quantitative

(extent, routes, timing, etc.) variation (Dingle 1996). Nowhere

is this variation more apparent than among salmonids,

where migrants (e.g. sea trout) and residents (e.g. lake trout)

show a behavioural distinction that is linked to phenomenal

life-history differences. The migration option involves trade-

offs: salmonid migrants have access to a marine food supply

and grow faster, and as a result are more fecund. However,

they also run a higher mortality risk on their seaward journey,

and they start breeding one or two years later than resident

salmonids (Jonsson and Jonsson 1993). The various forms

among salmonids actually look different (in size, colour

and shape), but among other species external differences

between migrants and residents are not generally obvious.

Japanese sardine Sardinops sagax melanosticus can be

divided into two groups (Hiramoto 1991): a coastal group

that lives in bays and has a limited migration range, and an

oceanic group that displays extended seasonal migrations.

This species shows a correlation between growth and

migration range. If the South African sardine that engage in

the run form a separate race, they should display discern-

ible physical or physiological characters, and their behaviour

should be explained against current and perhaps past

environments. For the sardine run to be a successful and

repeatable strategy, as opposed to maladaptive behaviour, it

will surely be contingent on an overall advantage regarding

reproductive success, given the high mortality likely experi-

enced by fish engaged in the run. What are the biotic and

environmental conditions that might favour such a trade-off

of life-expectancy for reproductive success? If such a

trade-off exists, it must surely leave a discernible mark on

population structure and individual resource allocation.

Material and methods

Most of the evidence relating to the sardine run and the tests

proposed for the various hypotheses are based on material

and methods already used and described in this suite (van

der Lingen et al. 2010b) or in historical papers, and are

briefly described below.

Van der Lingen et al. (2010a) provide information on

catches of sardine by beach-seine nets along the KZN coast

during some years between 1965 and 2009. The total number

of catches sampled by month is not always available, but

data collected recently (2003–2009) suggest values ranging

from 1 to 98 hauls (SD 31.1). Van der Lingen et al. (2010c)

also supply information on some biological characteristics of

sardine sampled from KZN beach-seine catches, including

data on caudal length and age distributions, and meristic

and morphometric data, and compare these with similar

data collected during research surveys and from commercial

purse-seine catches taken elsewhere along the South African

coast.

Connell (2010) presents a monthly time-series of sardine

egg abundance data derived from weekly, surface ichthyo-

plankton samples collected from 1987 to the present off

Park Rynie (about 60 km south of Durban). Initially, samples

were collected from a site 4–5 km offshore in a water depth

of 40–50 m, but from early 1994 a second sample was also

collected from 500–800 m offshore (15 m water depth). This

sampling strategy is in contrast to sampling during large-scale

biomass surveys conducted from 1984 to 2007, during which

eggs were collected using a CalVET net (van der Lingen and

Huggett 2003) and, more recently, a continuous underway

fish egg sampler (CUFES; van der Lingen et al. 1998) along

cross-shelf survey transects.

O’Donoghue (2009) and O’Donoghue et al. (2010a, 2010c)

report on visual surveys of sardine and their predators during

the run, made from the shore, small planes and small boats

along the KZN coast from 1988 to 2005. Dudley and Cliff

(2010) report on the number of sharks captured by shark

nets deployed along the KZN coast and on the incidence of

sardine in their stomach contents.

Coetzee et al. (2010) describe the various acoustic and

biological sampling methods performed during the 2005

sardine-run survey conducted onboard the RS Africana in

association with a small inflatable boat that investigated

shallow waters. Amongst other data, hydro acoustic estimates

of sardine density, and length frequency measurements and

age data, were collected and processed. Oceanographic

data such as sea surface temperature (SST), current speed

and direction as well as chlorophyll a (Chl a) concentrations

were also analysed. Additional oceanographic data collected

during the 2005 survey are also presented by Roberts et

al. (2010), together with continuous current data recordings

from ADCP moorings deployed off Port Edward and Port

Alfred since 2005.

Satellite data were also used to examine spatial and

temporal patterns in SST and Chl a. SST monthly daytime

averages of the NOAA Pathfinder version 5 (V5; available

at http://data.nodc.noaa.gov/pathfinder) were processed to

provide a compilation of the data from the AVHRR sensor

at 4 km resolution (Kilpatrick et al. 2001). In order to avoid

coastal contamination and lack of data, the coastal SST

data were extracted for distances of 5–10 km from the coast.

Ocean colour data used to estimate Chl a concentration

were downloaded from the NASA Ocean colour group web

portal using Seadas software (http://oceancolor.gsfc.nasa.

gov/seadas/). Altimetry data were also downloaded from

the CCAR near-real time altimetry site (http://argo.colorado.

edu/~realtime/welcome/). In some Hovmöller diagrams the

monthly data were smoothed temporally and spatially.

Hypotheses about ultimate factors (Hu) and potential tests

Hypotheses related to ultimate factors that attempt to answer

the question why the sardine run occurs, and the tests of

these hypotheses, are listed in Table 2 and described below.

Hu1: The sardine run represents a subpopulation spawning

migration

Recent advances in fishery genetics dismiss the conventional

view that fish, especially those with pelagic early stages

and a highly mobile adult phase, tend to form geographi-

cally extended and genetically homogeneous populations

with limited local adaptation and speciation (see reviews in

Hauser and Carvalho 2008, Fromentin et al. 2009). Evidence

for some degree of subpopulation structuring in the southern

Benguela sardine population is accumulating, with studies of

distribution patterns at varying biomass levels (Coetzee et al.

2008) and observations of consistent spatial differences in

some biological characteristics (van der Lingen et al. 2009)

suggesting the presence of at least two subpopulations.

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 453

Hypothesis number

and name Description Source Tests

Hu1: Subpopulation

spawning migration

Seasonal spawning

migration of a

subpopulation

Baird (1971):

hypothesis rejected

by that author but

revisited in this paper

T1: Is the sardine run a migration?

T3: Are sardine engaged in the run phenotypically distinct from the

rest of the population?

T4: Does molecular genetics conÞ rm that sardine engaged in the

run are genetically distinct from the rest of the population?

T5: Is there evidence of active spawning by sardine in KZN waters?

T6: Is there evidence of a sardine nursery ground in KZN waters?

T7: Is there successful recruitment arising from individuals spawning

in KZN waters?

T8: Do all year classes of the subpopulation spawn in KZN waters

and only there (or at least never reproduce when mixed with the

rest of the population)?

Hu2: Juvenile

equatorward

migration

Juvenile sardine move

equatorward of their

nursery. Unknown

motivation; but this

behaviour exists in birds

(e.g. oyster catcher

Haematopus moquini)

General theory by

Davies (1956a,

1956b);

application to the

sardine run by

Armstrong et al.

(1987)

T2: Are Þ sh younger when found to the north, rather than to the

south, of their nursery area (West and East coasts)?

Hu3: East Coast

functionally discrete

adult assemblage

(FDAA)

The sardine runners

are an FDAA that has

adapted to speciÞ c

conditions off the East

Coast, and the run is

the spawning migration

of this FDAA

General theory by

Fletcher et al. (1994);

application to the

sardine run by van

der Lingen et al.

(2010b)

T1, T3, T4, T5 and T8: As above but not always with the same

expected result

T9: The KZN FDAA should not mix with other FDAAs

Hu4: Seasonal

extension of

habitat and feeding

migration

A band of cold and

rich coastal water can

provide a suitable

habitat during winter

Baird (1971),

Heydorn et al. (1978),

Armstrong et al.

(1991)

T1: As above

T10: Test the permanence of this band in winter using satellite data

T11: Is there more food available in the KZN area during the

sardine run than farther south?

Hu5: Basin theory The area occupied

by the population is

proportional to its

abundance. More

favourable areas are

occupied Þ rst and less

favourable areas are

occupied only when

abundance is high

General theory by

MacCall (1990);

application to the

sardine run in this

paper

T12: Spatial analyses of abundance, occurrence of the sardine run

only at high biomass, most suitable habitat is occupied Þ rst

Hu6: Metapopulation The South African

(and Namibian)

metapopulation is

composed of local

populations that

were established by

colonists, survived

for a while, sent

out migrants, and

eventually disappeared

General theory by

Levins (1968);

application to the

sardine run in this

paper

T13: Make use of the criteria listed in Table 3

Hu7: Relic behaviour There was a favourable

and active spawning

area on the East Coast

in geological time.

Although it disappeared

long ago, genetic

inertia results in it still

being used by part of

the population

General theory by

Wyatt et al. (1991);

application to the

sardine run in this

paper

T1 and T3–T8: As above

T14: Palaeogeography, palaeoclimatology and

palaeosedimentology

Table 2: Hypotheses on ultimate factors pertaining to the sardine run: description, key references and potential tests (T)

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings454

A ‘western’ subpopulation that is distributed to the west of

Cape Agulhas and an ‘eastern’ subpopulation distributed to

the east have been postulated (de Moor and Butterworth

2009a). The existence of these two putative subpopulations

is supported by results from separate assessment models

(de Moor and Butterworth 2009b), and from coupling an

individual-based model of larval drift to a 3D-hydrodynamic

model of the southern Benguela (Miller et al. 2006), which

indicated that sardine life-history strategy could be divided

between two main systems, separated at Cape Agulhas.

Regardless of the existence of the two abovementioned

subpopulations, sardine participating in the KZN sardine run

could represent the seasonal spawning (gametic) migration of

another discrete sardine subpopulation. This hypothesis was

assessed in earlier research (e.g. Baird 1971) by comparing

some biological characteristics of KZN sardine with those

sampled from commercial catches made off the Western

Cape (see T3 in Table 2). Variability in phenotypic charac-

teristics may be due to genetic factors or environmental

influences, and is usually associated with the geographical

region occupied by a subpopulation (Begg and Waldmann

1999). Baird (1971) rejected the hypothesis of an East Coast

subpopulation after comparing length–mass relationships,

mean length at age, vertebral counts and otolith morphology,

finding no difference between sardine from KZN and those

from the Western Cape. He concluded that sardine partici-

pating in the KZN sardine run were migrants from the Cape

subpopulation, and were ‘...probably spawned in areas

with a similar environment and during the same season’

as sardine from the Cape. That conclusion was supported

by subsequent workers (Heydorn et al. 1978, Armstrong

et al. 1987, 1991). Grant (1985) also rejected this hypoth-

esis following results from electrophoresis analysis (see T4,

including all genetics approaches).

To further test the hypothesis of a subpopulation gametic

migration, it will be necessary (i) to ensure that the sardine

run is a migration, according to the definition and attributes

provided in the Introduction (see T1), and (ii) test if sardine

engaged in the run are genetically distinct from the rest of

the population, using modern molecular approaches (T4).

Assessing whether or not the sardine run is a spawning or a

feeding migration can be tested by looking for the presence

of sexually mature individuals in the area and, even better,

by sampling ichthyoplankton for eggs and larvae in the KZN

area (T5, and see reviews in Connell 2001, 2010). To test

the hypothesis of a substock it will be necessary to obtain

evidence of a nursery area in, and successful recruitment

arising from spawning in, KZN (T6) and to assess whether

cross-reproduction between subpopulations does not occur

or is limited enough to secure genetic differentiation. This

implies that all year classes of the putative subpopulation

spawn in KZN, and only there (allopatric spawning), or at

least never reproduce when mixed with the rest of the popula-

tion (sympatric spawning with seasonal segregation; T7).

Hu2: Juvenile sardine move equatorwards of their nursery

worldwide

Early research (Davies 1956a, 1956b) suggested an equator-

ward movement of juvenile pilchards (= sardine) from the

southern Benguela nursery grounds and a poleward move-

ment of adult fish when sexually mature, based on the slightly

smaller modal size classes in Namibian catches compared

to Cape catches in the 1950s. Davies postulated that the

sardine run on the East Coast was also an expression of this

equatorward movement. However, Newman (1970) rejected

this theory based on extensive tagging exercises in Namibia

(141 000 fish) and South Africa (74 344 fish), which suggested

largely separate populations in the northern and southern

Benguela. Fish from the Lüderitz area mingled with fish from

the Walvis Bay area, and only a very small proportion of

these fish actually moved to the southern Benguela. Sardine

in St Helena Bay remained in the southern Benguela and did

not move northward to Namibia at all, according to Barange

et al. (1999).

To further test Hu2, one can determine whether fish to the

north of their nursery areas are younger than those found on,

or to the south of these areas, both on the west and east

coasts of South Africa (T2 in Table 2).

Hu3: The sardine run represents an East Coast functionally

discrete adult assemblage

The concept of functionally discrete adult assemblages

(FDAAs) was initially proposed by Fletcher et al. (1994) who

hypothesised that two centres of spawning by Australian

sardine Sardinops sagax neopilchardus observed off Albany

and Bremer Bay on the south coast of Western Australia

(WA) could represent separately functioning adult populations

that were not reproductively isolated. A subsequent analysis

by Gaughan et al. (2001) provided further evidence for the

existence of three distinct centres of sardine spawning off the

southern Western Australian (WA) coast (off Albany, Bremer

Bay and Esperance) that were joined by areas of lower

spawning activity along a continuous distribution. Because

the spawning centres were distinct rather than strictly

separate, Gaughan et al. (2001) termed these groups FDAAs.

Regional differences in age compositions and gonadosomatic

indices of sardine from WA indicated that there was little or

no wide-scale mixing of mature age classes between the

three spawning centres (Gaughan et al. 2002). Those authors

further hypothesised that the persistence of these FDAAs

arose from phenotypic (as opposed to genetic) fitness-

related ties to localised areas of higher habitat suitability. In

contrast to the subpopulation hypothesis, the different FDAAs

share the same genetic pool because their individuals come

from a common pool of earlier stages, as for instance the

‘juvenile pool’ (Gaughan et al. 2001). Based on egg distribu-

tion patterns, the Transkei coast and KZN south coast could

represent a centre of sardine spawning that is distinct from

spawning centres off the West Coast and South Coast (van

der Lingen and Huggett 2003). Following Gaughan et al.

(2002), van der Lingen et al. (2010b) suggest that this could

indicate that fish participating in the KZN sardine run may be

an FDAA that has shown a phenotypic adaptation to specific

conditions off the East Coast. The run could represent the

spawning migration of an East Coast FDAA, with sardine

displaying behavioural patterns (in this case an eastward

migration) and possibly phenotypic adaptation that are

different to those displayed by FDAA(s) that remain on the

Agulhas Bank and spawn there in winter, although all these

FDAAs would come from a common pool of earlier stages.

Most of the tests that can be used for the FDAA hypothesis

are the same as those usable for the subpopulation (Hu1)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 455

hypothesis, with expected results being opposite in some

cases but in others similar. As for Hu1, sardine from the run

are expected to be phenotypically distinct from the rest of

the population (T3), but genetically indistinct from it (T4).

Both hypotheses imply evidence of active spawning in KZN

waters (T5), but in contrast to Hu1, there is no need for a

nursery area there (T6), nor the need for successful recruit-

ment related to spawning off the KZN coast (T7) to support

the FDAA hypothesis. The need for all year classes of the

putative KZN FDAA to spawn in KZN waters (T8) is shared

between Hu1 and Hu3. There is a specific test for the FDAA

hypothesis, directly related to its definition, which is that the

KZN FDAA should not mix with other FDAAs (T9).

Hu4: The sardine run arises from a seasonal extension of

habitat and is a feeding migration

Southern African sardine are known to prefer temperatures

between 14 and 20 °C (Barange et al. 1999), with those

along the East Coast previously observed in temperatures

below 20 °C (Baird 1971, Heydorn et al. 1978). The seasonal

occurrence of sardine along the East Coast during the winter

led Armstrong et al. (1991) to conclude that the sardine

run was a seasonal extension of sardine habitat due to the

favourable cooling of coastal and continental shelf waters

(i.e. a climatic migration). This hypothesis was tested (T10) by

comparing evidence of sardine run events with a time-series

of remotely sensed SSTs.

Sardine dietary carbon intake along the South African east

coast appears to be derived predominantly from zooplankton

(Mketsu 2008), chiefly calanoid copepods, with phytoplankton

rarely important (van der Lingen et al. 2010c). A paucity of

data pertaining to zooplankton abundance during the sardine

run precludes an investigation into whether sardine move up

the East Coast to occupy more favourable feeding conditions.

Any attempt to use remotely sensed Chl a concentration as

a proxy for sardine diet would need to be based upon an

established relationship between Chl a concentration and

zooplankton abundance. To our knowledge, this relation-

ship has not yet been established along the South African

east coast. A further caveat is the as yet untested accuracy

of remotely sensed Chl a concentrations within East Coast

waters. Nonetheless, despite these restrictions, sardine distri-

bution was compared with a remotely sensed Chl a concen-

tration time-series along the South African east coast (see

T11). Testing whether there is more food available along

the KZN coastline than farther south during the sardine run

would allow a decision regarding the possibility of the sardine

run being part of a seasonal feeding (alimental) migration.

Obviously, to be supported, both the climatic and alimental

migration hypotheses developed here must display all the

attributes of a migration (T1).

Hu5: The sardine run can be explained by the basin model

theory

According to basin model theory, the density and distributional

area occupied by marine fish are related to their biomass,

and fish movement can be implicitly considered as ranging

rather than migrating. This is an extension of the concept of

‘density-dependent-habitat-selection’ (DDHS) and the ‘ideal

free distribution’ (IFD) of Fretwell and Lucas (1970), in which

population size and density influence the choice of habitat,

and therefore also the distribution of the population among all

potential habitats, so as to optimise individual fitness (MacCall

1990). Specifically, MacCall (1990) portrayed this model of

fish density and distribution as an irregular basin, the shape

of which could potentially vary over time, filled with a liquid

under the influence of gravity. In this basin, habitat suitability

increases downward in each of the habitats and the depth

of the liquid at any location is proportional to the density-

dependent reduction in realised suitability at that location and

is also proportional to local density. Because densities tend to

be highest toward the centre of a species’ range, the deepest

area of the basin (i.e. the highest realised basic suitability)

will be central, and the topography will become progres-

sively shallower towards the periphery. The total volume of

liquid in the basin is related to total population size. Dynamics

leading to realisation of spatial distribution equilibrium arise

from movement orientated to gradients in habitat suitability

(viscosity) and rate of movement orientated to gradients in

population density (diffusivity). Per capita growth rate (fitness)

influences both the rate of population growth and migratory

flow, i.e. individuals are rewarded by increased reproductive

value for responding to a habitat-suitability gradient. It is worth

noting that habitat suitability/fitness is not well defined (see

review in MacCall 1990) and could possibly be used in the

context of maximisation of reproductive output, which could

translate into MacCall’s per capita growth rate.

A feature of the sardine run is that it seems to involve

only a small fraction of the sardine population at its fringe.

The following aspects of the basin theory are tested in

terms of the sardine run (T12): changes in population size

result in contraction or expansion of the population range,

so that at low biomass individuals occupy habitats with the

highest suitability, whereas at high biomass other, previously

less suitable, habitats become equally attractive and are

colonised, providing for population range expansion.

Hu6: The sardine run represents the behaviour of a meta-

population

The concept of metapopulations was first proposed by

Levins (1968) as ‘a population of local populations which

were established by colonists, survive for a while, send out

migrants, and eventually disappear. The persistence of

a species in a region depends on the rate of colonisation

successfully balancing the local extinction rate’. Levins (1968)

defined the metapopulation as:

there are a large number of sites, each supporting a 1.

single local population;

each local population has a probability of going extinct 2.

that may depend on its genetic composition;

the allele frequencies are governed by the classical 3.

genetic equations; and

vacant sites are recolonised by migrants from within the 4.

metapopulation.

The concept was then enriched with new ideas and

summarised by McQuinn (1997) when he applied it to

populations of Atlantic herring Clupea harengus. He synthe-

sised Levins’s ideas as ‘The population structure of many

species can be considered as an array of local populations

linked by variable degrees of gene flow’.

Another point is that continuous populations cannot be

considered as metapopulations. Kritzer and Sale (2004)

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings456

define a metapopulation as ‘a system of discrete local

populations, each of which determines its own internal

dynamics to a large extent, but with a degree of identifi-

able and nontrivial demographic influence from other local

populations through dispersal of individuals’ (Figure 1).

Hanski (1999) provides a list of 12 conditions necessary to

fulfil the status of metapopulation, and F Gerlotto (IRD, pers.

comm.) completed this list with four additional conditions

expressed by other authors (Table 3). We assessed

these 16 conditions with regard to present knowledge of a

putative sardine metapopulation off southern Africa (T13)

with two local populations potentially located off the coast

of Namibia, at least in historical periods of high abundance

(Bakun 2005), and three local populations off the coast of

South Africa (van der Lingen et al. 2010c). The three South

African local populations considered were: West Coast

and Western Agulhas Bank; Eastern Agulhas Bank; and

KwaZulu-Natal.

Hu7: The sardine run is relic behaviour

Carscadden et al. (1989) found that the only stock of

capelin Mallotus villosus that was not an intertidal spawner

was selecting areas of gravel deposition corresponding

to ancestral beaches of the Wisconsin glaciation period.

Wyatt et al. (1986) noted that the unusually deep location

of spawning grounds for sardine Sardina pilchardus off

North-West Europe is in an area that was coastal during the

post-Pleistocene transgression. These two examples show

that habitat selection during spawning can be the result of

remote ultimate factors that have resulted in what could be

termed relic behaviour, i.e. behaviour that was the norm in

some previous climate regime (e.g. a glacial period) but,

while still occurring, is no longer the norm in the present

regime (e.g. Romero 1985). A subpopulation of sardine on

the east coast of South Africa could potentially have been

brought about through a combination of bet-hedging and/

or relic behaviour (Coetzee et al. 2010). The relic behaviour

could have arisen with a northwards shift of polar conditions

and population separation during the last ice age and glacial

maximum some 16 000 years ago, when sea level was

approximately 130 m lower than at present (Miller 1990). At

that time, the southern extremity of the continental landmass

was 200 km farther south than the present day, subtropical

SSTs were 4 °C or more lower, the Subtropical Convergence

(STC) was farther north, the Agulhas Current retroflection

was farther eastwards, and there was little or no exchange

between the Indian and Atlantic oceans (Hutchings 1992,

Peeters et al. 2004, Parkington 2006). Each of these or a

combination thereof, together with the northward shift in cool

polar conditions, may have enforced separation of sardine

off the West and South coasts, with each having their own

independent spawning patterns and/or migrations. The end

of the ice age would have seen the west and east subpopu-

lations being reconnected with South/West Coast spawning

becoming dominant, possibly as a result of higher levels

of productivity in that region. A similar sequence of events,

borne out by molecular genetic studies, may have led to

the differentiation of the Atlantic and Indian populations

of albacore Thunnus alalunga (Chow and Ushiama 1995,

Viñas et al. 2004, AJ Penney, National Institute of Water &

Atmospheric Research, New Zealand, pers. comm.).

Relic behaviour has been demonstrated elsewhere. The

diadromous life histories of most anguillid eels and salmonids

are thought to have arisen from ‘migration loops’ expanding

away from low-productivity, food-poor origins in the tropical

marine and cold temperate riverine environments respec-

tively (Tsukamoto et al. 2002, Inoue et al. 2010). In both

families, the ‘ancestral loops’, including spawning migrations,

have been retained. The East Coast sardine ‘spawning

run’ differs from anguillid and salmonid relic behaviour by

not being dominant but, similarly, may have been partially

driven by higher productivity in this region during the glacial

periods. Relic behaviour may not necessarily arise over a

single glacial period but over successive ones, becoming

reinforced and more stable within each cycle (Kawanabe

1977). It follows that relic behaviour such as the East Coast

migration of sardine could be retained as an alternative stable

state to counter recurring glacial periods and by default be

a bet-hedge against biological and environmental pertur-

bations that befall the population on a shorter time-scale.

Nonetheless, to be retained in the genome of sardine, this

behaviour must be viable during the protracted interglacial

periods. This means that reproduction off the KZN coast must

be successful enough to produce recruitment to this subpop-

ulation, despite heavy predation during the sardine run.

Beyond the fact that the relic behaviour hypothesis is a

gametic migration of a subpopulation that must fulfil the five

attributes of a migration (T1) and also the other tests related

to the hypothesis of a subpopulation spawning migration

(Hu1; T3 to T8), this hypothesis is difficult to falsify. The

only specific tests that could allow differentiating it from Hu1

would be related to palaeogeography, palaeoclimatology

and palaeosedimentology (T14).

A. Network of closed populations

B. Metapopulation

C. Patchy population

Pro

babili

ty

Dispersal distance

Pro

babili

ty

Dispersal distance

Pro

babili

ty

Dispersal distance

Figure 1: Three types of spatially structured populations with general-

ised dispersion curves for each local population. Case A: closed local

population with no exchange between them; case B: metapopulation;

and case C: patchy population inside a single ‘super-population’.

The thicker lines represent the overall geographical limit of the

population(s). From Kritzer and Sale (2004)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 457

Hypotheses about proximate factors (Hp) and potential

tests

During the sardine run, sardine shoals need to swim along

the eastward-narrowing shelf of the Pondoland and Transkei

coasts against the fast, warm Agulhas Current to reach

KZN waters. In some years, the sardine have not reached

southern KZN or have arrived there late in the year. Here,

we list the hypotheses related to proximate factors (enabling

conditions) of the sardine run in an attempt to answer the

question relating to how the sardine run occurs (Table 4).

Hp1: Natal homing and imprinting

Natal homing is defined as the return of spawning adults

to their region of origin (Carr 1967), which in most cases is

allowed by imprinting of very early stages (larvae or even

eggs) by environmental cues (Stabell 1984). It differs from

spawning site fidelity in which fish may spawn for the first

time at a site different from where it was born. Natal homing

is a strategy that ensures the best chance of successful

reproduction. Adults return to natal sites to spawn irrespec-

tive of environmental change (the effects of which are likely

to be unpredictable to an animal), because that strategy is

likely to be most beneficial (in fitness terms) in the face of

environmental uncertainty. Natal homing is a strong driver

of genetic differentiation and it secures genetic isolation, by

preventing or limiting interbreeding. Although natal homing

could also be considered as an ultimate factor and environ-

mental cues associated to imprinting as proximate factors,

we classified it as a proximate factor because it is a process

that can be associated with two ultimate factor hypoth-

eses: the spawning migration of a subpopulation and relic

behaviour.

There are several examples of natal homing. Thorrold et

al. (2001) showed that between 61% and 80% of weakfish

Cynoscion regalis, an estuarine-spawning marine fish,

returned to their natal estuaries on the east coast of North

America after reaching sexual maturity offshore. Mature

Icelandic plaice Pleuronectes platessa were tagged on

spawning and feeding grounds off Iceland (Solmundsson

et al. 2005), and after weighting the number of recaptures

from standardised fishing effort, a minimum level of fidelity

to the spawning ground was estimated at 94% for the

spawning season one year after tagging. Fidelity of 72%

for the second and third spawning seasons was observed

after migrating from distant feeding grounds. The North

Atlantic bluefin tuna Thunnus thynnus has been shown to

consist of two fairly discrete populations, one based in the

Mediterranean and the other on the east coast of Canada

and the United States. Although they mix in feeding

aggregations as sexually immature fish in the North Atlantic

Bight (Rooker et al. 2008), the return of spawning adults

to their region of origin is high and remarkably similar for

both eastern and western spawning regions: 95.8% for the

Mediterranean, 99.3% for the Gulf of Mexico, 94.8% in the

Gulf of Maine and 100% in the Gulf of St Lawrence. Among

open-water coastal pelagic shoaling fish species, significant

isolation of stocks in the North Atlantic herring population

implies natal return to maintain such integrity (Stephenson

et al. 2009). Mullon et al. (2002) showed that observed

Metapopulation characteristics Relevance to the case of southern African sardine

1 Population size or density is significantly affected by migrations

Not obvious. At least this is not the case for migration between Namibia and South Africa due to the cold thermal barrier created by the Lüderitz upwelling cell (Lett et al. 2007)

2 Population density is affected by patch areas and isolation Yes, but mainly at a relatively small scale (clusters of schools)

3 Existence of asynchronous local dynamics Yes between Namibia and South Africa, but not between the three putative South African local populations

4 Population turnover, local extinctions and establishment of new populations

No, to the best of our knowledge

5 Presence of empty habitats Not permanent, except, to a certain extent, in the vicinity of the Lüderitz upwelling cell

6 Metapopulations persist despite population turnover Yes

7 Extinction risk depends on patch area No, except for Namibia.

8 Colonisation rate depends on patch isolation ? This condition seems irrelevant for large pelagic populations

9 Patch occupancy depends on patch area and isolation ? This condition seems irrelevant for large pelagic populations

10 Spatially realistic metapopulation models can be used to make prediction about metapopulation dynamics in particular fragmented landscape

? No specific modelling exercise done so far

11 Metapopulation coexistence of competitors ? Except possibly for the Namibian versus South African anchovy putative metapopulation

12 Metapopulation coexistence of prey and its predator ? This condition seems irrelevant for large pelagic populations

13 Evidence of genetic linkage ? Only electrophoresis analyses performed so far

14 Genetic or morphometric, meristic or biological/behavioural differences

Yes for morphometrics and meristics (similar to T3)

15 Existence of source/sink populations ?

16 Discrete local populations No

Table 3: List of characteristics describing a metapopulation (from Hanski 1999 for the first 12 conditions and F Gerlotto, IRD, pers. comm.,

for the last four) and assessment of their application to southern African sardine

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings458

anchovy Engraulis encrasicolus spawning patterns in the

southern Benguela Current system off South Africa could

be accurately reproduced by simulating a natal homing

reproductive strategy, i.e. individuals spawning at their natal

date and place.

Natal return would explain both the very small percentage

of the southern African sardine population that migrates

annually up the East Coast and into KZN waters, generally

considered to be about 10–15% (e.g. Armstrong et al.

1991), but as low as 1% when abundance is high (Coetzee

et al. 2010), and the fact that the intensity and occurrence

of the annual sardine run appears to bear no relationship

to the state of the overall population (see above). Whereas

it would seem reasonable to assume that fish arising from

successful spawning in KZN waters would tend to remain

at the eastern extreme of the distributional range of the

South African sardine population (Port Elizabeth to Cape

St Francis), recent focus on the adventure diving and tele-

vision documentary potential of the sardine run has seen

the development of early-season tracking of the eastward

movement of sardine shoals, with reports coming from as

far west as Mossel Bay (M Addison, Blue Wilderness Dive

Expeditions, pers. comm.).

The recent advance in knowledge of natal returns in

marine fish is largely as a result of the development of new

genetic (T4) and chemical techniques (described in T7). The

latter, in particular, has enabled detailed chemical tracking

of larval history, through the microchemistry of the growth

stages within the sagittal otoliths (ear bones). During their

migration along the Eastern Cape coast and into KZN

waters sardine spawn prolifically, but nothing is known of

the success or otherwise of this spawning in contributing to

recruitment to the southern African sardine population. The

natal return hypothesis relies on survival of recruits from the

spawning that occurs during the migration.

The most promising technique currently available to test

this hypothesis is to analyse the chemical constituents

of the core of the otoliths (T15) of juveniles from the four

major regions, namely the West Coast, the Agulhas Bank,

Algoa Bay and the KZN coast, in order to establish whether

juveniles can be separated by unique elemental constitu-

ents. If this proves to be the case, then analysis of the same

core area of adult fish participating in the annual sardine run

will establish what proportion of these adult fish are natal

returns, and provide other valuable insights into the structure

of the migrating shoals. If the run consists mainly of natal

returns, it will add a new dimension to management of the

resource, because preservation of within-species diversity is

an important element of an ecosystem approach to manage-

ment. Another test, although less powerful, could be based

on vertebral count data because it has been demonstrated

that this meristic characteristic depends on the temperature

experienced by larvae during the first few days following

hatching, with higher temperatures resulting in fewer

vertebrae (Ben Tuvia 1964, Andreu 1969). For instance,

young Sardina pilchardus found at the extreme equatorward

range of their distribution (14°43! N) had lower vertebral

counts than those from any other area in the Atlantic Ocean

(Fréon and Stéquert 1982).

Hp2: Are sardine pushed northward or shoreward by predators

Armstrong et al. (1991) proposed that the KZN component of

the sardine run is motivated by repeated attacks of predators

that would result in sardine being pushed northward and/or

Hypothesis number

and name Description Source Tests

Hp1: Natal homing and

imprinting

Fish return to the site of their

birth to reproduce because they

are imprinted at early stages by

environmental cues

Carr (1967), Stabell

(1984)

T15: Sardine engaged in the run are mostly born

in KZN waters

Hp2: Predator-driven

movement

Predators push sardine to the

north and/or to the shore once

arrived in Natal waters

Armstrong et al. (1991) T16: Fine-scale observations of predation and

response of sardine

Hp3: Environmental drive:

(a) favourable inshore

seasonal countercurrent

A seasonal onshore coastal

countercurrent (of the Agulhas

Current) would favour the

sardine run during all winter

Baird (1971) T17: Continuous coastal current measurement

(e.g. ADCP mooring line)

T18: Embedded, very high resolution numeric

model

Hp4: Environmental drive:

(b) favourable cooling of the

coastal area

Sporadic northward movement

of quanta of cooler waters

inshore along the East Coast

Heydorn et al. (1978) T18: As above

T19: Compare remotely sensed SST and

sardine run data (visual observations,

catches, eggs, acoustics) at high resolution

Hp5: Environmental drive:

(c) Waterfall Bluff gateway

During their north-east

displacement, sardine are

blocked by warm water flowing to

the south-west, north of Waterfall

Bluff, due to the topographic

configuration of this area. During

Natal Pulses the ‘gateway’

opens and the sardine run can

extend to the north-east

Armstrong et al. (1991),

Roberts et al. (2010)

T18: As above

T19: Look for the coincidence of Natal Pulses or

break-away eddies in remote-sensing data

with sardine run events

Table 4: Hypotheses on proximate factors pertaining to the sardine run: description, key references and potential tests (T)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 459

shoreward. Their evidence for this generalised statement was

the presence of sardine in warm water along this coastline. It

is difficult to test this hypothesis, because although there is a

very close association between sardine and their predators

(O’Donoghue et al. 2010a, 2010b, 2010c), particularly Cape

gannets Morus capensis and common dolphins Delphinus

capensis, it is uncertain whether the predators are following

or chasing their prey. Nonetheless, the application of

fine-scale observation techniques (T16), general knowledge

of fish behaviour and common sense could assist in reaching

a conclusion.

Hp3: Environmental drive: (a) favourable inshore seasonal

countercurrent

With little oceanographic information available, Baird (1971)

speculated that a well-established countercurrent inshore of

the Agulhas Current along the entire coast during winter could

be the prime cause of the sardine run. However, as pointed

out by Schumann (1987), the National Research Institute

for Oceanography (NRIO) measurements undertaken off

East London between April and December 1984, during

a year of substantial sardine catch on the Transkei/KZN

border, showed no indication of a defined seasonal counter-

current. From current meter data, Schumann (1987) sug-

gested that the mechanism by which sardine could be

assisted in their migration northwards occurred sporadi-

cally. This supported the views of Heydorn et al. (1978) who

were sceptical of the association of the sardine run with a

cool water countercurrent that originated off the southern

Cape and flowed up the East Coast in winter. Hp3 can be

tested by analysing data from ADCP moorings positioned

in shallow waters off the KZN coast (T17). Hydrodynamic

models in 3D with fine-scale resolution and one or two

levels of embedding (T18) could also aid in evaluation of this

hypothesis.

Hp4: Environmental drive: (b) favourable cooling of the

coastal area

Rather, Heydorn et al. (1978) thought it more likely that water

movement in the form of northward advection of pockets

(quanta) of cooler water inshore of the Agulhas Current

provided the physical mechanism for the run to occur. This

would be coupled with seasonal cooling of the inshore water

that is also conducive to the appearance of this temperate

species in KZN waters. Heydorn et al. (1978) also noted

that it is possible that a distinct nearshore regime may exist

within a kilometre from the shore. This region, which would

include the breaker zone, would probably be governed

by swell-driven mass transport and would reflect changes

in the wind field with a south-westerly swell generating

a northward nearshore current. To test this hypothesis,

fine-scale measurement of temperature, using, for instance,

high-resolution MODIS or aerial survey data, and relating

them to sardine run evidence, would be useful (T19). As

for Hp3, numerical models could help in demonstrating the

existence of quanta of cooler water (T18).

Hp5: Environmental drive: (c) Waterfall Bluff gateway hypothesis

The first dedicated attempt to assess and understand the

sardine run was undertaken by Armstrong et al. (1991)

using data from three ship-borne surveys along the East

Coast in August 1986, June 1987 and June 1990. They

observed sardine along the narrow Pondoland shelf as far

east as Port St Johns, but to the north of this the sardine

apparently descended into deeper, cooler water. Armstrong

et al. (1991) proposed that the sardine run is a phenomenon

arising from the expansion of the suitable environment for

this temperate species, during the cooler water conditions

that prevail in winter (Hp4) and, furthermore, that sporadic

current reversals and upwelling of cooler water onto the

narrow shelf results in the leakage of sardine schools along

the shelf between Port St Johns and Durban. Armstrong et

al. (1991) initially speculated that the Natal Pulse was the

key mechanism, but its intermittent occurrence (only found

20% of the year according to Lutjeharms and Roberts 1988,

or at intervals varying between 50 and 150 days according

to de Ruijter et al. 1999) meant that it could not be primarily

depended on for the sardine run.

Whereas the timing of current reversals between Port

Alfred and East London will slightly quicken or retard

progress of the sardine shoals moving up the East Coast, the

encroachment of the Agulhas Current onto the Pondoland

shelf is considered to be the first serious barrier for the

sardine shoals to overcome during their northward migration

to the KZN Bight. However, according to satellite imagery

(Roberts et al. 2010), this high-velocity warm temperature

barrier is quite variable and probably only impedes passage

for periods lasting several days. Anecdotal sightings

(O’Donoghue 2009) of sardine shoals near Waterfall Bluff

for extended periods, however, supports the earlier proposal

by both Schumann (1987) and Armstrong et al. (1991) of this

foremost barrier. According to Roberts et al. (2010), Natal

Pulses and break-away eddies provide the means for sardine

shoals to overcome this barrier and to move northward

along the narrow shelf, although their arrival on the KZN

south coast will depend on the timing of these features. The

process is schematically illustrated in their Figure 14, which

shows the ‘open gateway’ and ‘closed gateway’ situations,

with the latter allowing the shoals to reach the KZN south

coast and even Durban. They refer to these mechanisms

and their potential influence on the timing and appearance

of sardine in KZN waters as the ‘Waterfall Bluff gateway’

hypothesis.

Testing the existence and quantification of Natal Pulses

and break-away eddies can be partly addressed using

numeric models (T18), but a real test of Hp5 itself requires

the investigation of coincidental occurrences of Natal Pulses

or break-away eddies with sardine run events by combining

T17 and T19 approaches.

Results

Testing hypotheses

In this section, the tests listed in Tables 2 and 4 are reviewed.

They are dealt with separately from the hypotheses because

a given test can be applied to several hypotheses. Tests

already performed and documented in the literature are

recapitulated and updated when appropriate. Wherever

possible, new tests are performed and suggestions given

for further tests that could shed light on yet unanswered

questions, as methods are developed or data become

available.

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings460

T1: Is the sardine run a migration?

The five conditions listed in the Introduction that have to

be met before movement can be attributed to migration are

evaluated below.

T1a: Does the animal display persistent motion that takes

it beyond the home-range? The answer is definitely

yes. The sardine run is a seasonal displacement over

hundreds of kilometres.

T1b: Is the movement direct, and not erratic in direction?

Although the sardine run can be stopped (potentially

due to unfavourable environmental conditions farther

to the north-east; see below), the movement is always

direct and not erratic.

T1c: Does the animal pass suitable resources that would

otherwise not be overlooked? The answer to this

question is not obvious, except maybe at the onset of

the migration where sardine leave the relatively food-

rich eastern Agulhas Bank and enter into the poorer

food environment of the KZN coastal area (Hutchings

et al. 2010). Farther north, as sardine move past the

KZN Bight (limited observations by Pearce 1977),

they would encounter and pass suitable resources

originating from persistent upwelling in the region

between Richards Bay and St Lucia which spreads

southwards over the KZN Bight (Lutjeharms et al. 1989,

Hutchings et al. 2010).

T1d: Does the animal engage in specific departure and arrival

behaviour? Both the departure point and departure date

are variable but thought to be on the eastern Agulhas

Bank and generally sometime in May. Arrival in the area

north of Port Edward, as deduced from aerial surveys,

beach-seine catches, increased predator fish avail-

ability and rapid increase in the occurrence of sardine

eggs (O’Donoghue et al. 2010c, van der Lingen et al.

2010a, Fennessy et al. 2010 and Connell 2010 respec-

tively), occurs predominantly in June or July. There

is, however, little evidence of where sardine eventu-

ally go once they pass Durban (to the KZN Bight or

farther north?) and how long they remain off the KZN

coast, although sardine eggs are regularly collected

in samples taken off Park Rynie up until December

(Connell 2010). Whether sardine engage in any form

of display to signal departure or arrival, as is common

among migratory birds, is unknown. One may expect

changes in school structure, orientation, or feeding. The

test will require structured submarine observations that

have not yet been attempted, and indeed may not be

practical.

T1e: Are there physiological adjustments made to reserve

energy for a long journey? According to van der Lingen

et al. (2006), fish from the South Coast (20–27° E)

have a higher mean condition factor (CF) than those

from both the West (north of 33.5° S) and South-West

coasts. In contrast, sardine caught during the run

display a lower CF than in any other area (Coetzee

et al. 2010). Although CF is a complex indicator

reflecting not only condition but also morphology and

sexual maturation stage, these observations could be

interpreted as fish building up reserves on the South

Coast prior to departure and then quickly losing these

reserves as they migrate northwards along the KZN

coast.

From the above, it can be concluded that despite a few

uncertainties regarding mainly departure time and location,

as well as the ultimate arrival location, tests for confirming

the migration theory (T1) are largely positive.

T2: Are fish younger when found to the north (rather than

the south) of their nursery area?

Van der Lingen et al. (2010c; their Figures 6–8) show

that the age structure of sardine caught off the KZN coast

since 1955, although discontinuous, is dominated by

age classes 2–4. Age classes 0 and 1, although possibly

underestimated in beach-seine net catches, are seldom

abundant. Sardine caught in midwater trawls between

Port Alfred and Port Edward during the 2005 sardine run

survey were smaller in the south than farther northward

with no clear pattern in age structure (Coetzee et al. 2010).

Furthermore, van der Lingen et al. (2010c, Figure 2) show

that sardine caught off KZN typically ranged from 13 to

21 cm caudal length (CL) with an overall mode at 18 cm,

although bimodal structures are observed during some

years. The annual mean CL of KZN sardine caught by

beach-seines in recent years (1997–2005) appears to be

different from that of sardine caught by the purse-seine

fishery off Port Elizabeth during June and July of the same

years, with the KZN data showing less individuals of size

classes 16.0–18.0 cm and more of classes 18.5–19.5 cm

than the South Coast data (!2 test, p < 0.02; Figure 2).

Disaggregated commercial catches (beach seines) in

KZN in 2004 and 2005 compared to experimental catches

(midwater trawl) performed during pelagic spawner

biomass surveys during the same years show different

caudal length distributions (Figure 3), especially for young

fish, which is due to the different areas sampled (pelagic

spawner biomass surveys extend from Hondeklip Bay off

the West Coast to Port Alfred off the South Coast) and to

FR

EQ

UE

NC

Y (

%)

20

20 22 23 2421

15

10

5

12 13 14 15 16 17 18 19CAUDAL LENGTH (cm)

Port Elizabeth (n = 1 274)

Sardine run (n = 4 127)

Figure 2: Comparison between frequency distributions of caudal

length of sardine sampled from commercial purse-seine catches

taken off Port Elizabeth during June and July, and those sampled

from beach-seine catches taken off KZN during the sardine run, for

the period 1997–2005

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 461

different gear selectivity. Nonetheless, none of these data

support the notion that KZN sardine are younger than those

located farther south.

Barange et al. (1999) recorded a concentration of adult

sardine (and anchovy) on the spawning grounds on the

Agulhas Bank in summer, with nursery grounds on the West

Coast. As juveniles grow, they move back to the South

Coast and then disperse north and east as they grow older.

Barange et al. (1999) considered the stock on the East

Coast to be a small component of the total sardine popula-

tion. Figure 4 compares the distribution of sardine younger

or older than one year (using fish size as a proxy for age)

during winter surveys for four years of high recruitment

(2000–2003). Using years of high recruitment provides a

clearer representation of where the bulk of the 1+ year old

sardine had distributed themselves by the following summer.

From Figure 4 it is clear that in May fish are still migrating

southward from the West Coast nursery area (the recruitment

run), and by November have settled on the Agulhas Bank. It

does not suggest northward movement from nursery areas,

although, admittedly, surveys probably do not extend far

enough north eastward to rule this behaviour out completely.

In conclusion, the result of T2 obviously rejects Hu2 (juvenile

equatorward migration) for the West Coast and likely also for

the East Coast.

T3: Are sardine from the run phenotypically distinct from the

rest of the population?

Phenotypic differences between different components,

geographic and/or temporal strata, of a population can provide

indirect evidence for subpopulation structure, although they

cannot prove genetic isolation. Furthermore, phenotypic

differences can reflect prolonged separation of post-larval

stages in different environmental regimes.

Van der Lingen et al. (2010c) compared length–mass

relationships, vertebral counts, and morphometrics of sardine

from KZN with those from elsewhere off South Africa’s coast,

and found significant differences in condition factor, the

number of vertebrae and body shape that might be indica-

tive of the existence of a discrete subpopulation off the East

Coast. However, those authors cautioned that whereas small

sample sizes and plausible alternative explanations for these

differences precluded confirmation of this hypothesis, they

could not invalidate it.

T4: Are sardine from the sardine run genetically distinct from

the rest of the population?

Modern molecular genetics allow for the detection of a high

degree of heterogeneity in pelagic or semi-pelagic popula-

tions at geographical scales ranging from tens to a few

hundred kilometres, despite some degree of mixture or

2004

2005

Pelagic spawner biomass survey

Sardine run

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

FR

EQ

UE

NC

Y (

%)

20

15

10

5

20

15

10

5

CAUDAL LENGTH (cm)

Figure 3: Comparison between frequency distributions of caudal length of sardine sampled from KZN beach-seine catches during the

sardine run, and those sampled from midwater trawl catches during pelagic spawner biomass surveys conducted in October–December,

for 2004 and 2005. Distributions for sardine run samples are derived from all fish measured, whereas those for the survey samples are

acoustically weighted (i.e. weighted according to relative abundance per length class estimated from acoustic data)

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings462

close proximity of the spawning populations to each other

(see review by Hauser and Carvalho 2008). Estimates of

FST, the fraction of total genetic variation attributable to

differences among populations, is of particular interest in

this context. Indeed, FST estimates the relative decrease

in heterozygosity due to population substructure relative

to the expected heterozygosity in an equivalent panmictic

population. This kind of approach, not yet conducted in

South Africa at a spatial scale relevant for the sardine run,

is certainly one that could allow the best possible insight

for understanding the structure of the sardine population,

despite some limitations related to large populations. Ideally,

it would require simultaneous collection of samples at the

time of the sardine run from various locations along the

5

10

15

20

1 2 3 4 5 6 7 8 9AGE (years)

CA

UD

AL L

EN

GT

H (

cm

)

For each year, fish <1 year old in May were assumed to be

<12.5 cm and fish older than 1 but younger than 2 years in

November were assumed to be !12.5 and <16 cm

2000 2001

2002 2003

<1-year-olds in May

1- to 2-year-olds in November

<1-year-olds in May

1- to 2-year-olds in November

<1-year-olds in May

1- to 2-year-olds in November

<1-year-olds in May

1- to 2-year-olds in November

Sardine density (g m–2)

1 5 25 50 100

Figure 4: Density of sardine <12.5 cm CL in May and "12.5 and <16.0 cm CL in the following November for four years (2000–2003) during

which sardine recruitment was high (upper panel); and cut-off lengths for minimum and maximum caudal length of 1-year-old fish from the

sardine age–length curve (lower panel; courtesy D Durholtz, Department of Agriculture, Forestry and Fisheries)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 463

entire southern African coast, including Namibia. The ideal

distance between samples should be in the order of 100 km.

Coupling molecular genetics with otolith microchemistry (see

below) would increase the power of this approach.

T5: Is there evidence of active spawning in KZN?

The 21-year time-series of ichthyoplankton data collected

weekly from surface shelf waters at Park Rynie on the KZN

south coast since 1987 (Connell 2010) clearly demonstrates

that sardine spawn regularly in this area from June to

December. As expected with monospecific plankton data,

the dataset is dominated by zero values (78%) and extremely

skewed to the right (skewness = 370), to the point that

a lognormal transformation still provides an extremely

skewed distribution. Nonetheless, the dataset does not fit a

Pareto law. The most intense spawning occurred from June

to October (2.2–5.8 eggs m#3), despite some degree of

inter annual variability. Sardine egg concentrations off Park

Rynie, and those from near-surface samples collected along

the East Coast using a CUFES during the 2005 sardine

run survey (which ranged from 0 to 43.2 eggs m#3, and had

an average concentration of 0.6 eggs m#3 [SD 2.9] for both

survey phases combined; see Coetzee et al. 2010), are

substantially lower than those observed elsewhere off the

South African coast. Concentrations of sardine eggs collected

using a CUFES on the western Agulhas Bank ranged from

0 to 106.8 eggs m#3 and had an average of 5.0 ± eggs m#3

(SD 1.9) (van der Lingen et al. 1998), and similar average

and maximum concentrations have been observed in CUFES

samples collected off the West Coast (van der Lingen

and van der Westhuizen 2000) and South Coast (CDvdL

unpublished data).

The distance travelled between egg sampling sites and

the site of spawning can be roughly estimated from current

data and an estimation of the age of eggs collected. A

sardine egg takes about 24–36 h to hatch in warm waters

(King 1977), akin to the KZN south coast area during the

period June–December (average monthly AVHRR satellite

SST ranging from 19.5 to 25.8 °C). Egg stages vary from

freshly spawned to well developed, and on average eggs

can be estimated to be 12 h old (ADC pers. obs.). Current

direction in the sampling area off Park Rynie from June to

December is dominated by alongshore flow (to either the

north or south) and this pattern is consistent throughout the

year (results not shown). Semi-quantitative data on current

speed, backed-up by a few current meter measurements

from June to December 2006, indicate that the alongshore

current speed varied between 0.15 and 0.88 m s#1, with

an estimated average of 0.31 m s#1 regardless of their

estimated direction. According to these estimates, which

are in agreement with ship-borne (S–ADCP) measurements

(Roberts et al. 2010), the average distance travelled by an

egg in the alongshore direction can be estimated at 13 km,

varying from 6 to 38 km. Cross-shelf currents are seldom

observed in this area (1.8% inshore and 0.4% offshore) and

are much weaker, with speeds varying from 0 to 0.15 m

s–1. Therefore, the maximum distance travelled by an egg

in the cross-shelf direction can be estimated to be 6 km.

Intermediate current direction is dominated by south-inshore

currents (7.1%) whereas zero or undetectable currents

($0.1 m s–1) represent 6.1% of the dataset. These results

clearly confirm that the KZN area is an active spawning

area, with the possible exception of 2006 when no sardine

eggs were found in samples (Connell 2010).

Historical egg surveys conducted in KZN waters confirm the

spatial extent of spawning in this region (see Connell 2010)

as did the 2005 sardine run survey (see Figure 9 of Coetzee

et al. 2010). In conclusion, T5 is clearly positive, upholding

the hypothesis of active spawning in KZN and thereby

supporting Hu1 of a subpopulation spawning migration.

T6: Is there evidence of a nursery area off the KZN coast?

Connell (2010) gathered several lines of evidence from the

literature that supported the existence of a nursery area

in the KZN region, including the presence of early sardine

larvae (Beckley and Hewitson 1994, Beckley and Naidoo

2003), early juveniles (Heydorn et al. 1978, van der Byl

1980) and late juveniles (van der Byl 1978). Connell (2010)

concluded that locally spawned larvae may tolerate higher

temperatures on the KZN coast than elsewhere in South

Africa. Juvenile sardine were also found south of the KZN

region, from Port Edward to Port Elizabeth, as reported by

Miller et al. (2006) who linked the presence of these recruits

to local spawning. Nonetheless, one cannot exclude the

possibility that these individuals result from spawning in

KZN and farther northward, their transport or migration being

subsequently favoured by the dominant Agulhas Current.

Hence, the existence of a nursery area off the KZN coast is

likely.

T7: Is there successful recruitment attributed to individuals

spawned in KZN?

Whether or not all these early stages and juveniles contribute

significantly to recruitment of the South African sardine

population remains an unanswered question to date. Coetzee

et al. (2008) show that high sardine recruitment as a whole

is mainly associated with successful West Coast recruit-

ment, although the importance of recruitment emanating

from successful KZN spawning must be of significance in the

maintenance of a local spawning migration, particularly if it

results from a genetically distinct subpopulation. It is likely

that the use of otolith microchemistry, coupled with molecular

genetics, would provide a definitive answer to this question.

Indeed, otoliths take up several chemical substances and

their stable isotopes (e.g. strontium, strontium/calcium ratio,

barium, oxygen ["18O] or carbon ["13C] isotopes) in propor-

tion to their concentration in the ambient environment (review

in Fromentin et al. 2009). It is likely that there is a high

contrast in chemical tracers found in the Indian and Atlantic

oceans. Therefore, one can expect to trace the history of fish

movement from early stages to age at catch and to infer the

contribution of fish born in the Indian Ocean to the overall

population. Similarly, chemical tagging with tetra cycline or

isotopes, injected into mature females, has allowed identifi-

cation of returning recruits, by detecting the injected chemical

in the core of the returning juvenile otolith (Jones et al. 2005,

Almany et al. 2007). Nonetheless, the application of such

approaches are limited by the monetary expense of the

method per fish sampled, which would probably constrain

sampling to fewer individuals than required to obtain a precise

estimate of the contribution to recruitment of fish spawned in

KZN.

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings464

T8: Are all year classes of the subpopulation spawning in

KZN and only there (or at least never reproduce when mixed

with the rest of the population)?

Van der Lingen et al. (2010c; their Figures 6–8) show that

sardine caught by beach-seine off KZN since 1955 are

dominated by mature age classes (2- to 4-year-old fish) with

large interannual variability. Year classes 4, 5 and 6 are

often absent from samples, which can be attributed to a low

sampling rate, or to higher mortality than in the rest of the

population owing to repeated migrations through an area

with heavy predation pressure (see also general discussion

on this point).

200 400 600 80020 1 000

Onboard counts; n = 1 461

Eggs m!2

Hondeklip Bay

Cape TownMossel Bay

Port Elizabeth

Port Alfred

East London

Port St Johns

Port Edward

Durban

(a)

16° E 18° E 20° E 22° E 24° E 26° E 28° E 30° E

30° S

32° S

34° S

36° S

32° E

Hondeklip Bay

Cape TownMossel Bay

Port Elizabeth

Port Alfred

East London

Port St Johns

Port Edward

Durban

16° E 18° E 20° E 22° E 24° E 26° E 28° E 30° E

30° S

32° S

34° S

36° S

32° E

Eggs m!3

(b)

Min. = 0; Max. = 163.5

100 m

200 m

100 m200 m

Figure 5: (a) Composite distribution of sardine eggs (areal abundance expressed as eggs m–2) around the South African coast derived from 8 016

CalVET net samples collected during 24 annual pelagic spawner biomass surveys from 1984 to 2007 (updated from van der Lingen and Huggett

2003); (b) distribution of sardine eggs (volumetric abundance expressed as eggs m–3 at 6 m depth; symbol size proportional to concentration)

derived from CUFES samples collected during the 2008 spawner biomass survey (CDvdL unpublished data; note that the figure is generated

from onboard counts which require laboratory validation). The solid line in (a) indicates the maximum survey coverage (note that not all surveys, in

particular those during the early years, attained this coverage), and dashed ellipses on both maps indicate the location of spawning centres possibly

indicative of functionally discrete adult assemblages or subpopulations; 100 and 200 m isobaths are shown

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 465

The main spawning area of the South African sardine

population has alternated between being located predom-

inantly off the West Coast and predominantly off the

South Coast (van der Lingen and Huggett 2003; Figure 5),

with interannual and mostly interdecadal changes in its

location. The spawning season is protracted, occurring

year-round but mainly from August to late March, with two

peaks: September–October and February–March (van

der Lingen and Huggett 2003). Therefore, despite a large

temporal overlap between spawning in the KZN area and

in the rest of the sardine habitat that would allow allopatric

spawning, three months (June–August) out of five of the

main spawning season in the KZN area occur outside of the

peak spawning in the rest of the country, which prevents us

from excluding the possibility that the same fish reproduce

first off KZN and then on the Agulhas Bank. If this was

the case, it would make it difficult (but not impossible, if

fine spatio-temporal scales are involved) to observe the

existence of sympatric spawning with seasonal segrega-

tion. However, intense sardine spawning on the shelf edge

off Mossel Bay (see Figure 5) has been observed during

research surveys conducted in autumn (May/June; García

Fernández et al. 2008), and spawning there was also

observed in July 2005 immediately after the 2005 sardine

run survey (van der Lingen et al. 2005). In any case, due to

the protracted spawning season in the different areas and

the high swimming capacity of sardine, Test 8 is difficult to

perform and only indirect evidence (molecular genetics) can

contribute to addressing it.

T9: The KZN FDAA should not mix with other FDAAs

The putative KZN FDAA is obviously separated from other

putative FDAAs during the sardine run, but the fate and

whereabouts of sardine that survive the run is unknown.

Connell (2010) suggests that survivors move back down

the coast to the Agulhas Bank with the onset of summer,

based on the substantial presence of eggs in KZN up to

November and December, although this fact does not

inform on migration. If, instead of using log-transformed

data untransformed data are used, a clear decrease in egg

abundance is observed in September (Figure 6), which

could reflect the average transition period between the

onward migration (June–August) and the return migration

(November–December or later if fish move back without

spawning). However, the strong skewness of the egg distri-

butions precludes testing the significance of the decrease

of egg abundance in September. The average occurrence

of eggs in samples does not show a strong bimodal

pattern. Nonetheless, there is no evidence of adult sardine

in the KZN area and farther north during late summer

(March–April), and sardine are very seldom observed off

KZN from January to May (Connell 2010, O’Donoghue et al.

2010a, 2010c, van der Lingen et al. 2010a), which can be

explained in part by the unsuitable range of water tempera-

tures off the coast of KZN and Mozambique (Figure 7) at this

time of year. Therefore, it is very likely that sardine partici-

pating in the sardine run mix with other sardine after the run,

which means that the answer to T9 is negative.

T10: Test the permanence of a band of cold water in winter

The regular, annual observations of sardine during June

between East London (33° S) and Waterfall Bluff (31.5° S)

reported by O’Donoghue (2009) occurred along a stretch of

coastline undergoing seasonal cooling, with the exception of

a few years (2001, 2002, 2006 and 2007) in which coastal

waters failed to cool to below sardine’s upper tempera-

ture limit of 22 °C (Coetzee et al. 2010; see Figure 7). One

could consider that the seasonal range extension hypoth-

esis is supported in this region by the arrival of sardine

when sea conditions cool locally during the sardine

run. Indeed, evidence of large interannual variability in

the degree of cooling of shelf temperatures in the area

between Waterfall Bluff and Durban is coincident with high

inter annual variability in sardine sighting rates, as observed

during aerial surveys (Table 4 in O’Donoghue et al. 2010a)

conducted between May and August. Although sighting rate

and SST were found to be inversely associated across all

months within zones and across all zones in May, Figures

8 and 9 and Table 5 show that high sighting rates did not

always occur during periods of low temperatures (e.g.

1989, 2003) and that the relationship between SST and the

various sardine run indices does not hold when considering

averaged values available between June and August, except

for catches. Along this stretch of coastline, sardine tend to

move closer inshore, often to within 1 km of the surf zone

(O’Donoghue et al. 2010a). In doing so, they move beyond

the detection range of satellites, raising the possibility that

nearshore conditions are cooler than those measured farther

offshore by satellite. Sardine distribution has previously

been compared with SST measured at the KZN Shark

Board’s meshing installations, approximately 300 m from the

shoreline throughout this region (O’Donoghue et al. 2010c).

From that dataset, SST was included in a multi parameter

model investigating sardine presence as a function of

various environmental variables, and was shown to be a

significant variable, although it contributed little to explaining

sardine presence compared to current direction (from north

to south) and month effect (O’Donoghue et al. 2010c). This

result suggests that sardine presence is favoured by cooler

conditions, but does not support the permanence of a band

of cold water in winter.

50

100

150

200

250

300

350

J F M A M J J A S O N DMONTH

ME

AN

NU

MB

ER

OF

EG

GS

50

100

150

200

NU

MB

ER

OF

OB

SE

RV

AT

ION

SMeanObservations

Figure 6: Mean number of eggs per month collected in the Park

Rynie area from 1987 to 2009 and total number of monthly observa-

tions (updated series of Connell 2010, untransformed)

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings466

Additionally, the 4 km resolution used to create the satellite

image SST time-series possibly masks smaller-scale

features of the sardine distribution. For instance, in 2006, few

sardine were observed north of the Mbhashe River (32.2° S)

whereas dense aggregations of feeding predators were

observed off Morgan Bay (32.5° S, O’Donoghue 2009). In

this case, the predator-feeding aggregations coincided both

temporally and spatially with the confluence of cool upwelled

water and warm Agulhas Current water, as evidenced from

satellite imagery that clearly depicted a thermal front in this

region. But again this suggests that the presence of cooler

water is ephemeral, allowing us to conclude that T10 is

negative.

T11: Is there more food available in the KZN area during the

sardine run than farther south?

The remotely sensed Chl a concentration time-series (Figure

10) clearly shows that the cool conditions to the south of

SST (°C)

1980

1990

2000

YE

AR

SST (5–10 km) Shark catches Sardine catches Sightings of sardine Sardine eggs

MONTH

1971

2009

1980

1990

2000

1971

2009

Catches (number) Catches (kg0.3) Sightings (%) 0

Log (eggs+1)

F A J A O D F A J A O D F A J A O D F A J A O D F A J A O D

20 22 24 >26 0 200 400 600 0 20 40 0 2 4 6 8 0.5 1.0 >2.0

Figure 8: Hovmöller diagrams of the mean monthly SST values (AVHRR data, including second pixel from the coast) in the coastal band

30°–32° S and approximately 5–10 km from the coast, compared to different monthly indices of the occurrence and intensity of the sardine

run. Diagonal lines represent missing data. The vertical line is located on 1 June. Method and original data (although displayed differently)

are available in Dudley and Cliff (2010) for shark catches; van der Lingen et al. (2010a) for sardine catches; O’Donoghue et al. (2010a) for

sardine sightings; and Connell (2010) for sardine eggs

16

18

20

24

26

28

22

29° S

30° S

31° S

32° S

33° S

Thukela River

Durban

Mdoni

Waterfall Bluff

Mbhashe River

East London

Port Alfred

Port St Johns

SST (°C)1982 1984 1986 1988 1992 1994 1996 19981990 2002 2004 2006 20082000

YEAR

Figure 7: Hovmöller plot of SST data from Pathfinder, V5 (4.5 km resolution) from the AVHRR sensor, from 28° to 34° S along the East

Coast, 1985–2009. Contours indicate the 21 and 22 °C limits; the vertical bars indicate 1 August of each year. To increase the number of

available data the second pixel from the coast was retained

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 467

Waterfall Bluff contain higher concentrations of Chl a (although

the link between Chl a and zooplanktonic sardine prey has yet

to be validated). Between Durban and Waterfall Bluff there is

little evidence of increased primary productivity, suggesting

poor feeding conditions for sardine during this section of the

run. It is only in the KZN Bight that phytoplankton is more

abundant than in the Port Alfred area during the sardine run,

but the sardine run as an event is largely considered to end

off Durban (unless an unseen proportion moves through to

the Thukela Bank). This suggests that the fish move from

relatively good feeding conditions south of Mbhashe River to

poor conditions north of Waterfall Bluff. Thus, the notion of

the sardine run being an alimental migration is not supported

by Chl a data.

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

"2

"3

"10

1

23

"2

"1

0

1

2

"2"1

01

234

"2

"1

0

1

2

"3

"2"1

01

23

"3"2"1

0

1

32

"2

"3

"1

0

1

2

SST

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Shark catches

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Catches

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Sightings

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Eggs

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Egg proportion

1965 1968 1971 1974 1977 1980 1983 1986 1989 1992 1995 1998 2001 2004 2007

Shark stomachs

YEAR

RE

SID

UA

LS

Figure 9: Normalised interannual anomalies of SST and different indices of the occurrence and intensity of the sardine run averaged from

June to August only. Diamonds indicate missing data

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings468

From the analyses of plankton data collected during the

2005 sardine run survey, Coetzee et al. (2010) concluded

that primary and secondary productivity levels in the KZN

area are much lower than elsewhere on the western and

eastern Agulhas Bank. Furthermore, the lower condition

factor of sardine on the East Coast, compared to the

long-term average for fish caught on the West and South

coasts (van der Lingen et al. 2006), further supports the

idea that feeding conditions on the East Coast are not ideal,

although this decrease could be attributed to the cost of

migration (van der Lingen et al. 2010c).

T12: Spatial analysis of abundance

Before testing whether or not the basin theory can be used

to explain the occurrence of the sardine run, it is necessary

to first conceptualise the design of the basin for the South

African sardine population. A hypothetical model that depicts

the available habitat of sardine in terms of the concepts

provided by MacCall 1990 (Figure 11), and which incorpo-

rates information on changing productivity (Hutchings et al.

2010) and observed sardine distributional patterns (Coetzee

et al. 2008), suggests that the basin topography should

allow for two basins. There are two reasons why: levels of

primary and secondary productivity tend to be higher on the

West Coast and western Agulhas Bank than farther east,

and data from biomass surveys conducted since 1984 show

that some sardine are located on the less productive South

Coast even at low biomass levels. If range expansion of the

sardine population was based entirely on density-dependent

habitat selection (DDHS), it would be expected under a

single-basin scenario that sardine would be restricted to

the most productive West Coast system at low biomass.

Furthermore, Coetzee et al. (2008) showed that the area

occupied by sardine in the area west of Cape Agulhas was

relatively smaller at the same level of biomass than the area

to the east of Cape Agulhas. In terms of the above theory,

SSTShark

catches

Sardine

catches

Sighting

rate

Log

(eggs+1)

Egg

proportion

Shark

stomachs

SST 1 0.546 0.008** 0.883 0.132 0.579 0.320

Shark catches #0.130 1 0.572 0.876 0.969 0.387 0.005**

Sardine catches #0.538 0.102 1 0.052 0.578 0.494 0.124

Sighting rate 0.038 0.040 0.548 1 0.218 0.221 0.095

Log (eggs+1) 0.323 0.010 0.141 0.306 1 0.000** 0.084

Egg proportion 0.122 #0.211 0.172 0.303 0.827 1 0.079

Shark stomachs #0.257 0.594 0.356 0.529 0.519 0.526 1

Table 5: Correlation matrix of annual normalised mean values of SST and different indices of sardine run occurrence and intensity (same as

in Figures 8 and 9). Note that the correlations were computed using all available data for a given couple of variables, regardless of missing

values in other variables in the same year (variable degrees of freedom). Due to their highly skewed distribution, egg data are analysed

according to two modalities: their mean number and their mean proportion of presence in samples. Correlation coefficients appear below the

diagonal and p-values above; ** indicates statistical significance at the 1% level

53

210.5

0.20.1

CHL a(mg m!3)

60

20

10

Thukela River

1998 1999 2000 2001 2002 2003 2004

Durban

Mdoni

Waterfall BluffPort St Johns

Mbhashe River

East London

Port Alfred

YEAR

Figure 10: Chlorophyll a concentration between Port Elizabeth and Richards Bay, 1998–2005. The solid and dashed vertical lines denote the

1 June and 1 September respectively for that year (adapted from O’Donoghue et al. 2010a)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 469

this would suggest that the area west of Cape Agulhas can

accommodate higher densities and is thus more suitable

than the area east of Cape Agulhas. Additionally, Coetzee

et al. (2008) reported that the central Agulhas Bank area

off Cape Agulhas is only inhabited at very high levels of

biomass, hence the shallow topography of the basin model

in that area. The hypothetical model also considers the

thermal limits to sardine expansion farther northwards,

both on the West Coast, where the Lüderitz upwelling cell

is a permanent barrier to further expansion north westward

(Lett et al. 2007) and on the East Coast, where increasing

temperatures in the vicinity of Port St Johns during summer

(Armstrong et al. 1991, Roberts et al. 2010) prohibit further

expansion of sardine into the coastal region of KZN. The

position of both these temperature barriers is variable,

dependent on the intensity of upwelling off Lüderitz on the

West Coast, and on seasonal changes in the dynamics

of the Agulhas Current, which strongly influences coastal

temperatures on the East Coast.

Having established a likely hypothetical model, it is possible

to evaluate some of the basin theory attributes, originally

put forward by MacCall 1990, in the context of the South

African sardine population, which enable evaluation of the

proposed tests.

The total area occupied by sardine during November

during the period 1984–2007 was calculated from distribution

maps of sardine obtained from acoustic biomass surveys

and related to changes in sardine biomass during the same

period for both the entire population (Barange et al. 2009)

and separately for sardine in the area west and east of Cape

Agulhas (Coetzee et al. 2008). These studies both showed

that contraction and expansion of the sardine distributional

range were related to sardine abundance, consistent with

MacCall’s basin theory. Nonetheless, despite this consist-

ency with basin theory, this expansion and contraction

cannot explain the occurrence of the sardine run. From the

hypothetical model (Figure 11), expansion into the area east

of Port St Johns would only be possible in times of very high

sardine biomass, because the suitability of this area is low

relative to the rest of the shelf area. It is therefore reasonable

to conclude that the basin theory does not account for the

occurrence of the run because sardine have been present in

KZN waters even at times when the biomass of the sardine

population was very low.

Additionally, it is unlikely that DDHS alone influences the

distribution of sardine. Sardine distribution patterns from

biomass surveys reveal that even at very high biomass

levels, large productive areas of the West Coast are void of

sardine, whereas densities in less productive areas of the

South Coast are high (Figure 12). This is contrary to the

DDHS theory because fish increasing their fitness through

selection of the most suitable available habitat will do better

KZN coast(low suitability)

Maximumcarryingcapacity

Cold thermal barrier

shifts slightly north or

south throughout the

year, depending on

upwelling intensity

Hig

h s

uitabili

ty

Modera

te s

uitabili

ty

Warm thermal barrier

shifts north-east in

winter and south-west

in summer

Low sardine biomass

(1984–1997 and 2005–2009):

no sardine run expected

Medium sardine biomass

(1998–2004):

no sardine run expected

High sardine biomass

(2002–2003):

sardine run expected

Port St JohnsCape AgulhasLüderitz

Figure 11: Hypothetical basin model of the habitat available to the South African sardine population (top panel) at various levels of biomass

(fullness; bottom panel)

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings470

by migrating north-westwards up the West Coast instead

of north-eastwards up the East Coast. This argument also

holds in the context of improved reproductive value (better

transport of early stages to the West Coast nursery grounds

than compared to farther east; Miller et al. 2006) or in the

context of competition with anchovy (predation pressure on

sardine eggs spawned on the South Coast is likely to be

higher there compared to farther west).

November 2003

November 1986

200 m

200 m

Hondeklip Bay

Doringbaai

Cape Town

Mossel Bay

Port Elizabeth

Port Alfred

Port St Johns

30° S

31° S

32° S

33° S

34° S

35° S

36° S

37° S17° E 18° E 19° E 20° E 21° E 22° E 23° E 24° E 25° E 26° E 27° E 28° E 29° E

Hondeklip Bay

Doringbaai

Cape Town

Mossel Bay

Port Elizabeth

Port Alfred

Port St Johns

30° S

31° S

32° S

33° S

34° S

35° S

36° S

37° S17° E 18° E 19° E 20° E 21° E 22° E 23° E 24° E 25° E 26° E 27° E 28° E 29° E

Sardine density (g m"2)

1 5 25 50 100 500

(a)

(b)

Figure 12: Relative density and distribution of sardine during (a) the pelagic spawner biomass surveys of 1986 (low biomass) and (b) 2003

(high biomass)

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 471

T13: Series of specific tests related to metapopulations

Table 3 shows the characteristics describing a metapopu-

lation and assessment of their application to southern

African sardine. Given the uncertainty regarding application

for many of them, and conflicting responses in others, this

hypothesis cannot be validated, but seems unlikely.

T14: Palaeogeography, palaeoclimatology and palaeo-

sedimentology

Figure 13 compares the SST during the Last Glacial Maxi-

mum (LGM) 18 000 years ago and at present, and shows

the expansion of the southern part of the African continent

as a result of a much lower sea level in the past. It also

shows for both periods the estimated location of sardine-

suitable habitat. The offshore extent of the habitat is based

on about the 200 m isobaths at present and an approxi-

mation of the LGM situation, although this assumption is

debatable. For instance, in the California and the Humboldt

upwelling ecosystems, the very same Sardinops sagax

is found farther offshore than in the Benguela (Fréon et al.

2009). The northern extent of suitable habitat is set to the

22 °C SST isotherm, and the southern extent to coincide with

the inshore extent of the Agulhas Current. It seems unlikely

that the position of the Agulhas Current during the LGM

would have differed much from the present day, although

it probably would have been more intense and retroflected

farther east with increased recirculation of warm Agulhas

water into the southern Indian Ocean (Peeters et al. 2004). In

addition to a possible separation of sardine off the West and

South coasts, as mentioned above, this map suggests that

two large continental-shelf areas could have been inhabited

by sardine off the present Mozambique during the LGM.

These coastal areas, enriched by terrestrial nutrient input,

could have been favourable nursery areas and the sardine

LGM

18000 years agoPresent

Ice

Ice

Suitable habitat

Continental extentat low sea level

22

20

18

16

16

16

22

20

18

16

26

24

22

20

18

26

24

22

20

18

26

24

12

10

14

1210

14

0

20° S

40° S

60° S

0

20° S

40° S

60° S

20° E 40° E 20° E 40° E

Durban Durban

LEGEND

(a) (b)

Figure 13: Sea surface temperature (°C) and estimated sardine habitat (see text for details) during (a) the Last Glacial Maximum (LGM)

(18 000 years before present, redrawn from Stanley 1989), and (b) at present (winter). Also shown is the expansion of the southern part

of the African continent as a result of much lower sea level during the last ice age. The continental expansion southward is redrawn from

Parkington (2006) and the temperatures in (b) were drawn from a global SST map (100 km resolution) downloaded from a NOAA website

(www.osdpd.noaa.gov/data/sst/contour/global100.fc.gif) at the beginning of June 2010

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings472

run could be a relic spawning migration to the small remains

of this spawning ground: the KZN Bight and adjacent areas.

This scenario is speculative, and further tests should include

at least searching for evidence of sardine presence off the

present Mozambique during the LGM, which could be investi-

gated in core sediments providing that conditions preserved

fish remains (scales, vertebrae, etc.).

T15: Are sardine run fish mostly born in KZN?

Otolith microchemistry should also provide an answer to the

question of natal homing. Under this hypothesis, the chemical

composition of the core of the otoliths should be repeated

during every reproductive season, but possibly excluding the

first one (see Discussion).

It is noteworthy that vertebral counts of sardine run fish

performed recently (van der Lingen et al. 2010c) were lower

than those from the rest of the population. Notwithstanding

the limited number of samples, the finding that sardine

collected from the KZN coast had lower vertebral counts

than elsewhere along the South African coast supports the

idea that sardine run individuals were hatched in warmer

waters than the rest of the sardine population, most probably

in the KZN area, supporting the natal return hypothesis.

Nonetheless, because Baird (1971) found no significant differ-

ences in his vertebral count, one cannot reach a firm conclu-

sion for this test.

T16: Fine-scale observations of predation

There is some circumstantial evidence to suggest that

sardine are not pushed northward by predators. Observations

of feeding predators off the East Coast indicate that only

common dolphins have the ability to herd their prey into a

‘baitball’ from which they can feed (SHO’D pers. obs.). A

comparison of sardine and predator sighting rates along

the South African east coast (see Figure 3 in O’Donoghue

et al. 2010a) indicates that common dolphin abundance

decreases markedly northwards of the Eastern Cape/

KZN border. Sardine movement towards shore peaks

along the stretch of coastline between Mdoni and Durban.

From that figure it is clear that predator sighting rates are

lower there than those farther south along the coast. The

peak in sardine shoreward movement does, however,

coincide with the shoreward intrusion of warm water from

the Durban Eddy, which can be measured as an increase

in temperature at the KZN Sharks Board meshing installa-

tions (O’Donoghue et al. 2010c), making this the more likely

cause for the shoreward movement observed in this region.

Furthermore, although it is possible that predators control

the movement of their prey during a few hours and over

a limited distance, it is unlikely that this process can work

around the clock during several days and over hundreds of

kilometres. Underwater footage of the sardine run released

in the media (e.g. the film Ocean) show that successful

attacks by predators mostly arise in the vertical plane, from

above in the case of gannets and from below in the case

of sharks and dolphins. Successful attacks in the horizontal

plane are performed in open water by predators circling

sardine. Straight attacks by sharks in shallow waters, as

illustrated in Figure 13 in Dudley and Cliff (2010), are likely

to be successful as well. However, because of the ‘fountain

pattern’, a circular movement around the detected danger

displayed by prey to maintain visual contact with their

predator (Hall et al. 1986), it is unlikely that predators will

be able to push sardine horizontally over long distances. In

conclusion, despite a lack of firm evidence against it, it is

unlikely that Hp2 is valid.

T17: Continuous coastal current measurement (e.g. ADCP

mooring line)

The ADCP mooring data collected near Port Edward in 2005

(Roberts et al. 2010) confirm high south-westward velocities

of 50–100 cm s–1 in the inshore region (30 m) of the shelf,

with bottom temperatures commonly exceeding 20 °C. Both

factors are likely to constitute a barrier to the sardine run,

and consequently allow rejection of the seasonal inshore

countercurrent hypothesis (Hp3). Most importantly, Roberts

et al. (2010) show that current reversals on the shelf are

associated with both the Natal Pulse and the more common

Durban break-away eddies, which are necessary conditions

for supporting Hp5.

T18: Embedded very high resolution numeric model

Embedded numerical hydrodynamics models in 3D (with

two or more levels) allow fine-scale studies of key areas of

ecological interest (e.g. Penven et al. 2006). Providing that

small-scale local atmospheric forcing and detailed bathym-

etry are available, such models can accurately reproduce

current structure, although in the case of the KZN area

the steep slope of the shelf and the proximity of the strong

Agulhas Current could generate some technical challenges.

A frame model and some medium-scale embedded

models already exist for the southern African region (Veitch

et al. 2009), from which such a small-scale model could be

constructed. This model would, at least, allow testing of the

permanence of a seasonal coastal countercurrent (Hp3),

the sporadic northward movement of quanta of cool water

inshore (Hp4), and the existence of Natal Pulses (Hp5).

However, validation of Hp4 and Hp5 will remain difficult at

present given limitations on the temporal resolution of data

related to past sardine run events.

T19: Compare remotely sensed SST and sardine run data

at high resolution

The results from Roberts et al. (2010) verified that, whereas

the Agulhas Current is the single-most dominant feature on

the east coast of southern Africa and strongly influences shelf

circulation, there are both stationary and transient eddies

that exist between Algoa Bay and Durban (e.g. between

Cape Padrone and Keiskamma River, East London and

Haga Haga, Rame Head and Waterfall Bluff, and Park Rynie

and Balito; see figures in Roberts et al. 2010) and result in

coastal countercurrents. This dismisses the hypothesis by

Heydorn et al. (1978) who proposed that water movement in

the form of northward advection of pockets (quanta) of cooler

water inshore of the Agulhas Current provided the physical

mechanism for the run to occur (i.e. Hp4).

The hydroacoustic survey data collected during the 2005

sardine run survey showed that between 18 and 22 June

(Leg 1) sardine were distributed between Algoa Bay and the

Mbhashe River, with the main shoals north of Haga Haga

(see Figure 10 in Coetzee et al. 2010). Satellite images

shown in Figure 11f of Roberts et al. (2010) indicate that the

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 473

Port St Johns–Waterfall Bluff cyclonic eddy was in existence

on 16 June, with the Agulhas Current encroaching close

to the coast near the Mbhashe River. Expanded views of

the SST depict warm water (~23 °C) drawn into the Port St

Johns eddy as a northward filament that formed a distinct

thermal front. The inshore boundary of the Agulhas Current

moved offshore near Haga Haga, where the highest fish

density was measured. Figure 11g in Roberts et al. (2010)

shows that on 25 June, the inshore boundary of the Agulhas

Current had moved slightly farther offshore resulting in

water of 21–22 °C near the coast. The close association

of sardine distribution with the inshore boundary of the

Agulhas Current off the Haga Haga coast suggested that

the northward movement of the sardine shoals (and other

small pelagic species) was controlled by the dynamics of the

Agulhas Current, i.e. the Pondoland encroachment barrier.

The oceanographic situation appeared to have remained

similar for the next 4–5 days with the Port St Johns–

Waterfall Bluff eddy re-established on the 28 June and

the cooler (21–22 °C) band of coastal water terminating

north of Waterfall Bluff at Mkhambathi. To the north of

this, 24 °C water was close to the coast, extending to

Durban, i.e. the gateway was closed. The hydroacoustic

survey data collected on the southward-bound Leg 2 by

Coetzee et al. (2010) showed that sardine distribution had

spread northwards past Waterfall Bluff but no farther than

Mkhambathi (Figure 11 in Coetzee et al. 2010). The close

association between the northern extent of the sardine distri-

bution and the inshore boundary of the Agulhas Current,

and, moreover, that no sardine were found north of the

Agulhas Current coastal disjuncture, suggested again that

the dynamics of the Agulhas Current control the northward

movement of the sardine shoals. The lateral movement of

the inshore boundary of the Agulhas Current (opening and

closing of the gateway) off Waterfall Bluff for the three-month

period May–July 2005 is schematically shown in Figure 14c

in Roberts et al. (2010), and clearly illustrates that the ‘gate’

was closed during the last days of June, when the survey

was conducted. However, a transient break-away eddy,

observed in the satellite data, soon followed and the gate

opened on 13 July.

In conclusion, Armstrong et al. (1991) proposed that

the Natal Pulse was the main mechanism for the sardine

shoals to move north of Waterfall Bluff, but they dismissed

the notion because of the infrequency of the pulses. They

were, however, unaware of break-away eddies, identified in

Roberts et al. (2010), but otherwise their theory (Hp5) was

correct.

Discussion

The sardine run has stimulated the imagination of scientists

over several decades, leading to the proposal of several,

often contradictory, hypotheses to explain its existence

(Table 6). In this study, these have in the first instance been

classified according to their cause (ultimate factors that may

explain why the sardine run occurs) and enabling conditions

(proximate factors that detail how this run can take place).

Tests of these hypotheses were also proposed (Tables

2 and 4) and, where possible, applied to existing data.

Interestingly, all hypotheses with the possible exception

of one (Hu7) were found potentially falsifiable or refutable,

which means that there is a logical possibility that they

can potentially be shown false by an observation or by an

experiment, which is of particular value in science (Popper

1962). Results from these tests are summarised in Tables

7 and 8 and suggest that none of the proposed hypoth-

eses can be confirmed beyond doubt. Nonetheless, our

results are coherent since Table 6 shows (a) that when any

given hypothesis is supported, that automatically means

rejection of any other hypotheses that are contradictory, and

(b) virtually all hypotheses that are supported (or at least

inconclusive) do not contradict each other. Most hypoth-

eses related to ultimate factors can be rejected and the

two hypotheses that are supported (Hu1 and Hu7) are not in

conflict (Tables 6 and 7).

Strong support emerged for one ultimate factor hypothesis

(Hu1) and one proximate factor hypothesis (Hp5). It is likely

Hypotheses Hu1 Hu2 Hu3 Hu4 Hu5 Hu6 Hu7 Hp1 Hp2 Hp3 Hp4 Hp5

Hu1: Subpopulation spawning migration – – – – – # # # # # #

Hu2: Juvenile equatorward migration – – # – # – – # # # #

Hu3: East Coast functionally discrete adult assemblage – – # – – – – # # # #

Hu4: Seasonal extension of habitat and feeding migration – # # # # – – # # # #

Hu5: Basin theory – – – # – – – – – – –

Hu6: Metapopulation – # – # – – – # # # #

Hu7: Relic behaviour # – – – – – # # # # #

Hp1: Natal homing and imprinting # – – – – – # # # # #

Hp2: Predator-driven movement # # # # – # # # – – –

Hp3: Environmental drive: (a) favourable inshore currents # # # # – # # # – – –

Hp4: Environmental drive: (b) favourable cooling of the coastal area # # # # – # # # – – –

Hp5: Environmental drive: (c) Waterfall Bluff gateway # # # # – # # # – – –

# Compatible

– Incompatible

Table 6: Compatibility of hypotheses

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings474

that the sardine run is the seasonal spawning migration of

a genetically distinct subpopulation of sardine that is found

mixed with other subpopulations during the rest of the year.

Although genetic and otolith microchemistry tests (T4, T7

and T15) are still needed to fully validate Hu1, this hypoth-

esis is supported by positive tests based on migratory

behaviour, phenotypic differences and evidence of different

spawning sites and nursery areas (T1, T3, T5 and T6). The

existence of several subpopulations with different migratory

behaviour is common in the animal kingdom and well known,

particu larly for some bird species where only a fraction of the

population performs a seasonal migration (Berthold 2001).

Such disparity could arise from a mixed behavioural strategy

of the species which results in an evolutionary stable

strategy.

Table 8 shows that only one hypothesis (Hp5) was

supported whereas another (Hp1) remains inconclusive,

but both hypotheses are not in conflict (Table 6). Indeed,

two complementary processes can explain how the sardine

run occurs despite the presence of several strong barriers

(ecological and environmental) to its success. The first one

is the likely (but as yet not fully tested) existence of a natal

homing strategy by sardine (Hp1) which, possibly due to

imprinting of environmental cues at an early stage of egg

and/or larval development, ensures that maturing individuals

migrate back to the place where they were spawned, guided

by physical or chemical signals. Fréon and Misund (1999)

believe that natal homing is more generalised than expected

in pelagic fish and suggested that permanent chemical

stimuli, related to the local marine ecosystem and/or

continental inputs (e.g. from rivers) present in the spawning

grounds, could provide the imprinting cues. The second

likely enabling process relates to the hydrography and its

influence on functioning of the so-called Waterfall Bluff

gateway (Hp5). SST satellite data and current ADCP data

show how hydrographic processes enable sardine passage

through a normally highly unfavourable thermal and current-

related barrier, aided by the sporadic presence of Natal

Pulses and break-away eddies. The Waterfall Bluff gateway

was unlikely to have been a constraint to the northward

migration of sardine shoals during the last glacial maximum,

and is probably only a current-enabling process that was

not present in the recent past. Hp5 is incompatible with Hp4

(cooling of the coastal zone) and the two hypotheses are

Hypotheses on ultimate factors T1 T2 T3 T4 T5 T6 T7 T8 T9 T10 T11 T12 T13 T14 Conclusion

Hu1: Subpopulation spawning migration##

*

#

**

…

***

##

**

#

**

…

***

0

***

Supported

**

Hu2: Juvenile equatorward migration––

***

Rejected

***

Hu3: East Coast functionally discrete adult

assemblage

##

*

#

*

…

*

##

**

0

**

–

***

Rejected

*

Hu4: Seasonal extension/feeding migration##

*

–

**

––

**

Rejected

**

Hu5: Basin theory–

**

Rejected

**

Hu6: Metapopulation–

**

Rejected

*

Hu7: Relic behaviour##

*

#

**

…

***

##

**

#

**

…

***

0

***

0

**

Supported

*

Result of the test: … to be performed; – negative; –– strongly negative; 0 inconclusive; # positive; ## strongly positive

Strength of the test and conclusion: * low; ** medium; *** high

Table 7: Different tests (Tn) applied to different hypotheses about ultimate factors (Hun) and corresponding results and final conclusion.

Note that the strength of a test may also differ according to the tested hypothesis. Blank cells mean that the test is not relevant for the

corresponding hypothesis

Hypotheses on proximate factors T15 T16 T17 T18 T19 Conclusion

Hp1: Natal homing and imprinting

…/0

*** Inconclusive

Hp2: Predators-driven movement–

**

Rejected

**

Hp3: Favourable inshore currents—

***

…

*

Rejected

**

Hp4: Favourable cooling of coastal area…

*

–

**

Rejected

*

Hp5: Waterfall Bluff gateway#

**

Supported

**

Table 8: Different tests (Tn) applied to different hypotheses on proximate factors (Hpn) and corresponding results and final conclusion (see

Table 7 for definition of symbols). Note that T15 has been performed twice for vertebral count data, and is still to be performed for otolith

microchemistry

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 475

tested differently (T10 and T11 versus T8 and T9 respec-

tively) due to differences in the processes involved and their

duration (short term for Hp5), although there are similarities

between the end result of each process.

The choice to migrate does not need to be a conscious

one and in the case of the sardine run, in which several

impediments and challenges to migration are encountered,

it probably is not. During the 2005 sardine run survey, one of

the authors (LH) jotted some wisdom down in his notebook

about conditions in KZN: ‘Line 20 Scottburgh, 25/06/2005,

3am. Very similar to line 16. Warm water, deep weak thermo-

clines, low concentrations of cells, flat particle spectra. Why

anything wants to live in this godforsaken place, let alone

migrate hundreds of km to get here in the face of incredible

predation, is quite beyond me. Life must be tough at home!’.

This aptly sums up the obstacles faced by migrating sardine

and suggests that only a strong instinctive behaviour, geneti-

cally hard-wired and generating automated responses to

sensory cues, can explain a counter-intuitive behaviour such

as the sardine run.

Analogies can be drawn with other spectacular natural

migrations such as the obstinate upstream migration of

salmon challenged by natural or artificial obstacles or the

‘trek of the Wildebeest’ (a migration of 1.5 million ungulates)

across the vast plains of Africa, relentlessly tracked by their

predators, in search of rain-ripened grazing. Such behaviour

has to be rewarding in terms of an individual’s reproduct ive

success. In the case of the sardine run the reward is

obviously not food-related, nor is it related to predator

avoidance. It is more likely that in depositing eggs upstream

of a recruitment ground, as do many other species in the

region (Hutchings et al. 2002), sardine will gain an advantage

for the survival of their offspring.

The hypothesis that the sardine run exists due to relic

behaviour (Hu7) inherited during the Last Glacial Maximum,

when one or several large sardine nursery areas were

likely located off the coast of the present Mozambique, was

also supported, mostly based on the same tests as those

performed for Hu1 because the hypotheses are closely

related. Indeed they both imply a seasonal migration of a

subpopulation, the only difference being that Hu1 does not

imply the existence of prehistoric distant nursery areas and,

conversely, Hu7 does not imply that present day spawning

on the KZN coast is highly rewarding in terms of repro ductive

success. Even so, for a subpopulation to have persisted for

the long periods of time implied by Hu7, it must have a viable

reproductive strategy. There is, however, at least one factor

that could counter the validity of Hu7 and to a large extent

Hu1 as well: if the same cohorts, after reaching maturity,

repeatedly take part in the sardine run up until the end of

their life (which is a prerequisite of Hu1 and Hu7), and if

mortality is much higher for the sardine run subpopulation

than for the rest of the population, then the age structure

of the former should be biased toward younger individuals.

Analyses of the few available data (van der Lingen et al.

2010c) do not tend to support this, although accurate ageing

of sardine is difficult (Durholtz 2005). Another explanation

could be that young adult sardine do not migrate during their

first or second season after attaining sexual maturity in order

to build up their resources and size in the south, such that

they are more likely to make a greater and more successful

contribution in the following year. This assumption is linked

to the fact that larger fish migrate farther, as discussed in

Coetzee et al. (2010). Further analyses of length and

age data would assist in either supporting or refuting this

hypothesis.

The similar length distributions for sardine >15 cm CL

obtained from commercial purse-seine catches and midwater

trawl catches when compared with beach-seine catches off

KZN (Figures 2 and 3) is interesting and could possibly result

from an interaction between the higher natural mortality rate

experienced during the sardine run being offset by a low

exploitation rate. Indeed, the average commercial catch of

sardine taken in KZN since the 1970s is <150 t year#1 (van

der Lingen et al. 2010a). If one assumes a sardine run

biomass of 30 000 t (Coetzee et al. 2010), this amounts to

an exploitation rate of only 2.5%, which is far lower than that

for the rest of the population (11% for the period 1987–2007,

Coetzee et al. 2008).

Some tests are so powerful (indicated by stars in Tables

7 and 8) that, had they been performed, they would have

allowed conclusive validation or rejection of some hypoth-

eses. This applies particularly for the molecular genetics

(T4) and otolith microchemistry (T7, T15) methods, and even

more so if the two approaches are applied concurrently on

the same individuals. Doing this would have allowed better

support of Hu1, Hu7 and their related proximate hypothesis

Hp1. Some other powerful tests were performed, but their

results were not always conclusive owing to data paucity,

the number of repetitions and technical issues related to

data collection. Improved datasets are advised. A difficulty

inherent in some potential tests (e.g. T19) is that the

different indices of the sardine run occurrence and intensity

are seldom in agreement with each other (Figure 8),

because they are inaccurate or were not computed at similar

temporal and spatial scales. For instance, in contrast to all

other time-series, egg data collected off KZN throughout

the year (Connell 2010) provide evidence not only of the

sardine run, but also of the fact that sardine remain off the

KZN coast, and reproduce there for several months until

their return migration in spring.

The return migration remains poorly understood and is

only evidenced by the presence of eggs in the vicinity of Park

Rynie long after the sardine run has occurred (Figure 6). It is

likely that sardine move back to the South Coast using the

fringe of the powerful Agulhas Current to aid migration at a

depth that is suitable in term of temperature. This strategy

should be energy saving and would strongly limit predation,

at least by birds.

Recommendations for future work that could improve

understanding of the sardine run include: (1) a combi na tion of

molecular genetics (T4) and otolith microchemistry (T7, T15);

(2) collection of further evidence of a sardine nursery ground

in the KwaZulu-Natal Bight area in summer; (3) employment of

high resolution (<1 km) satellite data to study oceanographic

conditions present in the inshore area; (4) repetition of ADCP

moorings and determination of oxygen content at strategic

sites along the KZN coast (T18), including shallow waters;

and contrast of ADCP records with evidence of sardine run

events. Further suggestions relate to improved knowledge on

palaeogeog raphy, palaeoclimatology and palaeosediment-

ology (T14); improved monitoring of commercial catches

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings476

during the sardine run to derive an index of abundance;

monthly acoustic surveys along the KZN coast to test for the

possible existence of a deeper northward migration of sardine

shoals to the KZN spawning area during June–July and to

gain knowledge about the return migration; or alternatively

perform stomach content analyses of predators in the KZN

area from mid-September to mid-December.

In conclusion, the efforts of the scientific community over

the past five decades, as summarised in van der Lingen

et al. (2010a), have substantially improved understanding

of ecological processes associated with this extraordinary

wildlife phenomenon. The basis of this paper was to evaluate

the validity of existing hypotheses, several of which were

generated at a time when the ecological processes affecting

the sardine run were poorly understood. Several of these

have now been rejected, and others can only be tested after

more data become available, or advanced techniques are

applied. These limitations notwithstanding, our approach

suggests that the sardine run is most likely a seasonal

spawning migration of a genetically distinct subpopulation

of sardine responding to a strong instinct of natal homing.

The mechanism enabling passage through unfavourable

thermal and current-related barriers is the sporadic presence

of Natal Pulses and break-away eddies that allow sardine to

migrate into a hostile environment to complete their life cycle

following successful spawning in KZN waters. In summary,

this subpopulation is likely to follow the conventional

triangular plan of migration (Harden Jones 1968) described

in our Introduction.

Acknowledgements — Laurent Drapeau (IRD, US 140 ESPACE,

France) is sincerely acknowledged for his contributions to satellite

data analysis and time-series analysis. Mike Armstrong (CEFAS)

is thanked for his comments on an early draft of the manuscript,

and George Branch (University of Cape Town) and an anonymous

referee are warmly acknowledged for their detailed and rapid reviews

of this paper.

References

Almany GR, Berumen ML, Thorrold SR, Planes S, Jones P. 2007.

Local replenishment of coral reef fish populations in a marine

reserve. Science 316: 742–744.

Andreu B. 1969. Las branquispinas en la caracterizacion de las

poblaciones de Sardina pilchardus (Walb.). Investigaciones

Pesquera 33: 427–523.

Armstrong MJ, Berruti A, Colclough J. 1987. Pilchard distribution

in South African waters, 1983–1985. In: Payne AIL, Gulland JA,

Brink KH (eds), The Benguela and comparable ecosystems.

South African Journal of Marine Science 5: 871–886.

Armstrong MJ, Chapman P, Dudley SFJ, Hampton I, Malan PE.

1991. Occurrence and population structure of pilchard Sardinops

ocellatus, round herring Etrumeus whiteheadi and anchovy

Engraulis capensis off the east coast of southern Africa. South

African Journal of Marine Science 11: 227–249.

Attwood CG, Cowley PD. 2005. Alternate explanations of the

dispersal pattern of galjoen (Dichistius capensis). South African

Journal of Marine Science 27: 141–156.

Baird D. 1971. Seasonal occurrence of the pilchard Sardinops

ocellata on the east coast of South Africa. Investigational Report,

Division of Sea Fisheries, South Africa 96: 1–19.

Bakun A. 2005. Seeking an expanded suite of management tools:

implication of rapidly-evolving adaptive response mechanisms (e.g.

“school-mix feedback”). Bulletin of Marine Science 76: 463–483.

Barange M, Coetzee J, Takasuka A, Hill K, Gutierrez M, Oozeki

Y, van der Lingen C, Agostini V. 2009. Habitat expansion and

contraction in anchovy and sardine populations. Progress in

Oceanography 83: 251–260.

Barange M, Hampton I, Roel BA. 1999. Trends in the abundance

and distribution of anchovy and sardine on the South African

continental shelf in the 1990s, deduced from acoustic surveys.

South African Journal of Marine Science 21: 367–391.

Beckley LE, Hewitson JD. 1994. Distribution and abundance of

clupeoid larvae along the east coast of South Africa in 1990/91.

South African Journal of Marine Science 14: 205–212.

Beckley LE, Naidoo AK. 2003. Exploratory trials with light-traps to

investigate settlement stage fishes in subtropical, coastal waters

off South Africa. African Zoology 38: 333–342.

Begg GA, Waldman JR. 1999. An holistic approach to fish stock

identification. Fisheries Research 43: 35–44.

Ben Tuvia A. 1964. Influence of temperature on vertebral number

of Sardinella aurita from Eastern Mediterranean. Israel Journal of

Zoology 12: 59–66.

Berthold P (ed.). 2001. Bird migration: a general survey (2nd edn).

Oxford: Oxford University Press.

Carr A. 1967 (ed.). So excellent a fish: a natural history of sea

turtles. New York: Schribner.

Carscadden JE, Frank KT, Miller DS. 1989. Capelin (Mallotus

villosus) spawning on the Southeast shoal: influence of physical

factors past and present. Canadian Journal of Fisheries and

Aquatic Sciences 46: 1743–1754.

Charnov EL. 1976. Optimal foraging, the marginal value theorem.

Theoretical Population Biology 9: 129–136.

Chow S, Ushiama H. 1995. Global population structure of albacore

(Thunnus alalunga) inferred by RFLP analysis of the mitochondrial

ATPase gene. Marine Biology 123: 39–45.

Coetzee JC, Merkle D, Hutchings L, van der Lingen CD, van den

Berg M, Durholtz MD. 2010. The 2005 KwaZulu-Natal sardine

run survey sheds some light on the ecology of small pelagic

fish off the east coast of South Africa. African Journal of Marine

Science 32: 337–360.

Coetzee JC, van der Lingen CD, Fairweather T, Hutchings L. 2008.

Has the fishery contributed to a major shift in the distribution

of South African sardine? ICES Journal of Marine Science 65:

1676–1688.

Connell AD. 2001. Pelagic eggs of marine fishes from Park Rynie,

KwaZulu-Natal, South Africa: seasonal spawning patterns of the

three most common species. African Zoology 36: 197–204.

Connell AD. 2010. A 21-year ichthyoplankton collection confirms

sardine spawning in KwaZulu-Natal waters. African Journal of

Marine Science 32: 331–336.

Cury P. 1994. Obstinate nature: an ecology of individuals. Thoughts

on reproductive behaviour and biodiversity. Canadian Journal of

Fisheries Aquatic Sciences 57: 1664–1673.

Davies DH. 1956a. The South African pilchard (Sardinops ocellata).

Sexual maturity and reproduction 1950–1954. Investigational

Report, Division of Sea Fisheries, South Africa 22: 1–155.

Davies DH. 1956b. The South African pilchard (Sardinops ocellata).

Migration 1950–55. Investigational Report, Division of Sea

Fisheries, South Africa 24: 1–52.

Dawson MN, Grosberg RK, Botsford LW. 2006. Connectivity in

Marine Protected Areas. Science 313: 43–44.

de Moor CL, Butterworth DS. 2009a. A 2-stock hypothesis for

South African sardine: two discrete stocks. Unpublished report,

MCM/2009/SWG-PEL/23. Cape Town: Marine and Coastal

Management, Department of Environmental Affairs and Tourism.

de Moor CL, Butterworth DS. 2009b. A two discrete stock hypothesis

for South African sardine resource. Unpublished report, MCM/2009/

SWG-PEL/47. Cape Town: Marine and Coastal Management,

Department of Environmental Affairs and Tourism.

de Ruijter, WPM, van Leeuwen PJ, Lutjeharms JRE. 1999.

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 477

Generation and evolution of Natal pulses: solitary meanders

in the Agulhas Current. Journal of Physical Oceanography 29:

3043–3055.

Dicken ML. 2010. Socio-economic aspects of boat-based ecotourism

during the sardine run within the Pondoland Marine Protected Area,

South Africa. African Journal of Marine Science 32: 405–411.

Dingle H (ed.). 1996. Migration. The biology of life on the move.

New York: Oxford University Press.

Dudley SJF, Cliff G. 2010. Influence of the annual sardine run on

catches of large sharks in the protective gillnets off KwaZulu-

Natal, South Africa, and the occurrence of sardine in shark diet.

African Journal of Marine Science 32: 383–397.

Durholtz D. 2005. Report on sardine age determination. Unpublished

report, SWG/AUG2005/PEL/06. Cape Town: Marine and Coastal

Management, Department of Environmental Affairs and Tourism.

Fennessy ST, Pradervand P, de Bruyn PA. 2010. Influence of the

sardine run on selected nearshore predatory teleosts in KwaZulu-

Natal. African Journal of Marine Science 32: 375–382.

Fletcher WJ, Tregonning RJ, Sant GJ. 1994. Interseasonal variation

in the transport of pilchard eggs and larvae off southern Western

Australia. Marine Ecology Progress Series 111: 209–224.

Fréon P, Arístegui J, Bertrand A, Crawford RJM, Field JC, Gibbons

MJ, Tam J, Hutchings L, Masski H, Mullon C, Ramdani M, Seret

B, Simier M. 2009. Functional group biodiversity in eastern

boundary upwelling ecosystems questions the wasp-waist trophic

structure. Progress in Oceanography 83: 97–106.

Fréon P, Misund OA (eds). 1999. Dynamics of pelagic fish distrib-

ution and behaviour: effects on fisheries and stock assessment.

Cambridge: University Press.

Fréon P, Stéquert B. 1982. Note sur la présence de Sardina

pilchardus (Walb) au Sénégal : étude de la biométrie et interpré-

tation. Rapports et Procès-verbaux des Réunions du Conseil

international pour l’Exploration de la Mer 180: 345–349.

Fretwell SD, Lucas HL. 1970. On territorial behaviour and other

factors influencing habitat distribution in birds. I. Theoretical

development. Acta Biotheoretica 19: 16–36.

Fromentin J-M, Ernande B, Fablet R, de Pontual H. 2009.

Importance and future of individual markers for the ecosystem

approach to fisheries. Aquatic Living Resources 22: 395–408.

García Fernández I, van der Lingen CD, Moloney C. 2008.

Characterization and comparison of autumn and spring

spawning habitat of sardine (Sardinops sagax) and round herring

(Etrumeus whiteheadi) on the Eastern Agulhas Bank, South

Africa. Symposium guide and book of abstracts, South African

Marine Science Symposium 2008, Cape Town, South Africa.

Cape Town: South African Network for Coastal and Oceanic

Research. pp 37–38.

Gaughan DJ, Fletcher WJ, McKinlay JP. 2002. Functionally distinct

adult assemblages within a single breeding stock of the sardine,

Sardinops sagax: management units within a management unit.

Fisheries Research 59: 217–231.

Gaughan DJ, White KV, Fletcher WJ. 2001. The links between

functionally distinct adult assemblages of Sardinops sagax: larval

advection across management boundaries. ICES Journal of

Marine Science 58: 597–606.

Gerkin SD. 1959. The restricted movements of fish populations.

Biological Reviews of the Cambridge Philosophical Society 34:

221–242.

Grant WS. 1985. Population genetics of the southern African

pilchard, Sardinops ocellata, in the Benguela upwelling system.

In: Bas C, Margalef R, Rubies P (eds), International symposium

on the most important upwelling areas off western Africa (Cape

Blanco and Benguela), Barcelona, 1983. Barcelona: Instituto de

Investigaciones Pesqueras. pp 551–562.

Hall SJ, Wardle CS, MacLennan DN. 1986. Predator evasion in a

fish school : test of a model for the fountain effect. Marine Biology

91: 143–148.

Hanski I. 1999. Metapopulation ecology. New York: Oxford University

Press.

Harden Jones FR. 1968. Fish migration. London: Edward Arnold

Publishers Ltd.

Hauser L, Carvalho GR. 2008. Paradigm shifts in marine fisheries

genetics: ugly hypotheses slain by beautiful facts. Fish and

Fisheries 9: 333–362.

Heydorn AEF, Bang ND, Pearce AF, Flemming BW, Carter RA,

Schleyer MH, Berry PF, Hughes GR, Bass AJ, Wallace JH, van

der Elst RP, Crawford RJM, Shelton PA. 1978. Ecology of the

Agulhas Current region: an assessment of biological responses

to environmental parameters in the south-west Indian Ocean.

Transactions of the Royal Society of South Africa 43: 151–190.

Hiramoto K. 1991. The sardine fishery and ecology in the Joban and

Boso waters of Central Japan. In: Kawasaki T, Tanaka S, Toba Y,

Taniguchi A (eds), Long-term variability of pelagic fish populations

and their environment. Oxford: Pergamon Press. pp 117–128.

Hutchings L. 1992. Fish harvesting in a variable, productive

environment – searching for rules or searching for exceptions?

South African Journal of Marine Science 12: 297–318.

Hutchings L, Beckley LE, Griffiths MH, Roberts MJ, Sundby S, van

der Lingen C. 2002. Spawning on the edge: spawning grounds

and nursery areas around the southern African coastline. Marine

and Freshwater Research 53: 307–318.

Hutchings L, Morris T, van der Lingen CD, Lamberth SJ, Connell

AD, Taljaard S, van Niekerk L. 2010. Ecosystem considerations

of the KwaZulu-Natal sardine run. African Journal of Marine

Science 32: 413–421.

Inoue JG, Miya M, Miller MJ, Sado T, Hanel R, Hatooka K, Aoyama

J, Minegishi Y, Nishida M, Tsukamoto K. 2010. Deep-ocean

origin of the freshwater eels. Biology Letters 6: 363–366.

Jones GP, Planes S, Thorrold SR. 2005. Coral reef fish larvae

settle close to home. Current Biology 15: 1314–1318.

Jonsson B, Jonsson N. 1993. Partial migration: niche shift versus

sexual maturation in fishes. Reviews in Fish Biology and Fisheries

3: 348–365.

Kawanabe H. 1977. Relic social structure hypothesis on the terri-

toriality of ayu, Plecoglossus altivelis (Pisces: Osmeridae).

Proceedings of the Japan Academy, Series B 53: 74–77.

Kennedy JS. 1985. Migration, behavioural and ecological. In: Rankin

MA (ed.), Migration: mechanisms and adaptive significance.

Contributions to the Marine Sciences 27: 5–26.

Kilpatrick KA, Podesta GP, Evans R. 2001. Overview of the NOAA/

NASA Advanced Very High Resolution Radiometer Pathfinder

algorithm for sea surface temperature and associated matchup

database. Journal of Geophysical Research 106(C5): 9179–9197,

doi:10.1029/1999JC000065.

King DPF. 1977. Influence of temperature, dissolved oxygen and

salinity on incubation and early larval development of the South

West African pilchard Sardinops ocellata. Investigational Report,

Division of Sea Fisheries, South Africa 114: 1–35.

Kritzer JP, Sale PF. 2004. Metapopulation ecology in the sea: from

Levins’ model to marine ecology and fisheries science. Fish and

Fisheries 5: 131–140.

Law RM. 2007. Fisheries-induced evolution: present status and

future directions. Marine Ecology Progress Series 335: 271–277.

Lett C, Veitch J, van der Lingen CD, Hutchings L. 2007. Assessment

of an environmental barrier to transport of ichthyoplankton from the

southern to the northern Benguela ecosystems. Marine Ecology

Progress Series 347: 247–259.

Levins R (ed.). 1968. Evolution in changing environments. Princeton,

New Jersey: Princeton University Press.

Lutjeharms JRE, Grundlingh ML, Carter RA. 1989. Topographically

induced upwelling in the Natal Bight. South African Journal of

Science 85: 310–316.

Lutjeharms JRE, Roberts HR 1988. The Natal Pulse: an extreme

transient on the Agulhas Current. Journal of Geophysical Research

Downloaded At: 21:50 16 November 2010

Fréon, Coetzee, van der Lingen, Connell, O’Donoghue, Roberts, Demarcq, Attwood, Lamberth and Hutchings478

93(C1): 631–646, doi:10.1029/JC093iC01p00631.

MacCall AD (ed.). 1990. Dynamic geography of marine fish popula-

tions. Seattle: University of Washington Press.

Mace GM, Harvey PH, Chutton-Brock TH. 1984. Vertebrate

home-range size and energetic requirements. In: Swingland IR,

Greenwood PJ (eds), The ecology of animal movement. Oxford:

Clarendon Press. pp 32–53.

McQuinn IH. 1997. Metapopulations and the Atlantic herring. Reviews

in Fish Biology and Fisheries 7: 297–329.

Miller DCM, Moloney CL, van der Lingen CD, Lett C, Mullon C,

Field JG. 2006. Modelling the effects of physical-biological

interactions and spatial variability in spawning and nursery areas

on transport and retention of sardine Sardinops sagax eggs and

larvae in the Southern Benguela ecosystem. Journal of Marine

Systems 61: 212–229.

Miller DE. 1990. A southern African Late Quaternary sea-level curve.

South African Journal of Science 86: 456–458.

Mketsu QK. 2008. Comparative dietary analysis of sardine and

other clupeids from presumed mixed shoals off South Africa’s

east coast. MSc thesis, University of Cape Town, South Africa.

Mullon C, Cury P, Penven P. 2002. Evolutionary individual-based

model for the recruitment of anchovy (Engraulis capensis) in the

southern Benguela. Canadian Journal of Fisheries and Aquatic

Sciences 59: 910–922.

Myeza J, Mason RB, Peddemors VM. 2010. Socio-economic

implications of the KwaZulu-Natal sardine run for local indigenous

communities. African Journal of Marine Science 32: 399–404.

Newman GG. 1970. Migration of the pilchard (Sardinops ocellata) in

southern Africa. Investigational Report, Division of Sea Fisheries,

South Africa 86: 1–6.

Noakes DLG. 1992. Behaviour and rhythms in fishes. In: Ali MA

(ed.), Rhythms in fishes. New York: Plenum Press. pp 39–50.

O’Donoghue SH. 2009. The sardine run: investigating sardine,

Sardinops sagax, and predator distributions in relation to

environmental conditions using GIS and remotely sensed products.

PhD thesis, University of KwaZulu-Natal, Durban, South Africa.

O’Donoghue SH, Drapeau L, Dudley SFJ, Peddemors VM. 2010c.

The KwaZulu-Natal sardine run: shoal distribution in relation to

nearshore environmental conditions, 1997–2007. African Journal

of Marine Science 32: 293–307.

O’Donoghue SH, Drapeau L, Peddemors VM. 2010a. Broad-scale

distribution patterns of sardine and their predators in relation to

remotely sensed environmental conditions during the KwaZulu-

Natal sardine run. African Journal of Marine Science 32:

279–291.

O’Donoghue SH, Whittington PA, Peddemors VM, Dyer BM 2010b.

Abundance and distribution of avian and marine mammal

predators of sardine observed during the 2005 KwaZulu-Natal

sardine run survey. African Journal of Marine Science 32:

361–374.

Parkington J (ed.). 2006. Shorelines, strandlopers and shell middens.

Cape Town: Krakadouw Trust.

Pearce AF. 1977. The shelf circulation off the east coast of South

Africa. CSIR Research Report No. 361. Stellenbosch: Council for

Scientific and Industrial Research.

Peeters FJC, Acheson R, Brummer GJA, de Ruijter WPM,

Schneider RR, Ganssen GM, Ufkes E, Kroon D. 2004. Vigorous

exchange between the Indian and Atlantic oceans at the end of

the past five glacial periods. Nature 430: 661–665.

Penven P, Debreu L, Marchesiello P, McWilliams JC. 2006.

Application of the ROMS embedding procedure for the Central

California Upwelling System. Ocean Model 12: 157–187.

Popper K (ed.). 1962. Conjectures and refutations: the growth of

scientific knowledge. New York: Basic Books.

Roberts MJ, van der Lingen CD, Whittle C, van den Berg M. 2010.

Shelf currents, lee-trapped and transient eddies on the inshore

boundary of the Agulhas Current, South Africa: their relevance to

the KwaZulu-Natal sardine run. African Journal of Marine Science

32: 423–447.

Romero A. 1985. Ontogenetic change in phototactic responses

of surface and cave populations of Astyanax fasciatus, Pisces.

Copeia 4: 1004–1011.

Rooker JR, Secor DH, De Metrio G, Schlosser R, Block BA, Neilson

JD. 2008. Natal homing and connectivity in Atlantic bluefin tuna

populations. Science 322: 742–744.

Schumann EH. 1987. The coastal ocean off the east coast of South

Africa. Transactions of the Royal Society of South Africa 46:

215–229.

Shields WM. 1984. Optimal inbreeding and the evolution of

philopatry. In: Swingland IR, Greenwood PJ (eds), The ecology

of animal movement. Oxford: Clarendon Press. pp 132–159.

Sinclair ARE. 1984. The function of distance movements in vertebrates.

In: Swingland IR, Greenwood PJ (eds), The ecology of animal

movement. Oxford: Clarendon Press. pp 240–258.

Smith RL (ed.). 1980. Ecology and field biology (3rd edn). New

York: Harper & Row Publishers.

Solmundsson J, Palsson J, Karlsson H. 2005. Fidelity of mature

Icelandic plaice (Pleuronectes platessa) to spawning and feeding

grounds. ICES Journal of Marine Science 62: 189–200.

Stabell OB. 1984. Homing and olfaction in salmonids: a critical

review with special reference to the Atlantic salmon. Biological

Review 59: 333–388.

Stanley SM. 1989. Exploring earth and life through time. New York:

Freeman WH and Company Ltd.

Stephenson RL, Melvin GD, Power MJ. 2009. Population integrity

and connectivity in Northwest Atlantic herring: a review of

assumptions and evidence. ICES Journal of Marine Science 66:

1733–1739.

Swingland IR. 1984. Intraspecific differences in movement. In:

Swingland IR, Greenwood PJ (eds), The ecology of animal

movement. Oxford: Clarendon Press. pp 102–115.

Thorrold SR, Latkoczy C, Swart PK, Jones CM. 2001. Natal homing

in a marine fish metapopulation. Science 291: 297–299.

Tinbergen N. 1963. On aims and methods of ethology. Zeitschrift

für Tierpsychologie 20: 410–433.

Tsukamoto K, Aoyama J, Miller MJ. 2002. Migration, speciation,

and the evolution of diadromy in anguillid eels. Canadian Journal

of Fisheries and Aquatic Sciences 59: 1989–1998.

Tyler JA, Rose KA. 1994. Individual variability and spatial

heterogeneity in fish population models. Review of Fish Biology

and Fisheries 4: 91–123.

van der Byl PCN. 1978. The annual Natal sardine run 1978.

Internal Report. Cape Town: Sea Fisheries Branch, Department

of Industries.

van der Byl PCN. 1980. The Natal sardine run. Annual Report No.

3. Cape Town: Sea Fisheries Institute, Department of Agriculture

and Fisheries..

van der Lingen CD, Checkley D, Barange M, Hutchings L, Osgood K.

1998. Assessing the abundance and distribution of eggs of sardine,

Sardinops sagax, and round herring, Etrumeus whiteheadi, on the

western Agulhas Bank, South Africa, using a continuous, underway

fish egg sampler. Fisheries Oceanography 7: 35–47.

van der Lingen CD, Coetzee JC, Hutchings L. 2010a. Overview of

the Kwazulu-Natal sardine run. African Journal of Marine Science

32: 271–277.

van der Lingen CD, Coetzee JC, Hutchings L (eds). 2010b. The

KwaZulu-Natal sardine run. African Journal of Marine Science

32: 269–479.

van der Lingen C[D], Coetzee J, Hutchings L, Peddemors V, Merkle

D, van den Berg M, van der Westhuizen J, Dyer B. 2005. Report

on the 2005 sardine run survey. Unpublished report, SWG/

AUG2005/PEL/04. Cape Town: Marine and Coastal Management,

Department of Environmental Affairs and Tourism.

van der Lingen CD, Durholtz MD, Fairweather TP, Melo Y. 2009.

Downloaded At: 21:50 16 November 2010

African Journal of Marine Science 2010, 32(2): 449–479 479

Spatial variability in biological characteristics of southern Benguela

sardine and the possible existence of two stocks. Unpublished

report, MCM/2009/SWG-PEL/39. Cape Town: Marine and Coastal

Management, Department of Environmental Affairs and Tourism.

van der Lingen CD, Fréon P, Fairweather TP, van der Westhuizen

JJ. 2006. Density-dependent changes in reproductive parameters

and condition of southern Benguela sardine Sardinops sagax.

African Journal of Marine Science 28: 625–636.

van der Lingen CD, Hendricks M, Durholtz MD, Wessels G,

Mtengwane C. 2010c. Biological characteristics of sardine caught

by the beach-seine fishery during the KwaZulu-Natal sardine run.

African Journal of Marine Science 32: 309–330.

van der Lingen CD, Huggett JA. 2003. The role of ichthyoplankton

surveys in recruitment research and management of South African

anchovy and sardine. In: Browman HI, Skiftesvik AB (eds), The big

fish bang: proceedings of the 26th annual larval fish conference.

Bergen: Institute of Marine Research. pp 303–343.

van der Lingen CD, van der Westhuizen JJ. 2000. Use of a

continuous, underway fish egg sampler in South Africa. In

Checkley DM Jr, Hunter JR, Motos L, van der Lingen CD (eds),

Report of a workshop on the use of the continuous underway fish

egg sampler (CUFES) for mapping spawning habitats of pelagic

fish. GLOBEC Report 14: 27–30.

Veitch J, Penven P, Shillington F. 2009. The Benguela: a laboratory

for comparative modelling studies. Progress in Oceanography

83: 296–302.

Viñas J, Alvarado Bremer JR, Pla C. 2004. Inter-oceanic genetic

differentiation among albacore (Thunnus alalunga) populations.

Marine Biology 145: 225–232.

Wyatt T, Cushing DH, Junquera S. 1991. Stock distinctions and

evolution of European sardine. In: Kawasaki T, Tanaka S,

Toba Y, Taniguchi A (eds), Long term variability of pelagic fish

populations and their environment. Oxford: Pergamon Press. pp

229–238.

Downloaded At: 21:50 16 November 2010

Downloaded At: 21:50 16 November 2010