Future marine Zooplankton research - a perspective.

Abstract

During the Second Marine Zooplankton Colloquium (MZC2) 3 issues were added to those developed 11 yr ago during the First Marine Zooplankton Colloquium (MZC1). First, we focused on hot spots, i.e., locations where zooplankton occur in higher than regular abundance and/or operate at higher rates. We should be able to determine the processes leading to such aggregations and rates, and quantify their persistence. Second, information on the level of individual species, even of highly abundant ones, is limited. Concerted efforts should be undertaken with highly abundant to dominant species or genera (e.g., Oithona spp., Calanus spp., Oikopleura spp., Euphausia superba) to determine what governs their abundance and its variability. Third, zooplankton clearly influence biogeochemical cycling in the ocean, but our knowledge of the underlying processes remains fragmentary. Therefore a thorough assessment of variables that still need to be quantified is required to obtain an understanding of zooplankton contributions to biogeochemical cycling. Combining studies on the 7 issues from MZC1 with the 3 from MZC2 should eventually lead to a comprehensive understanding of (1) the mechanisms governing the abundance and existence of dominant zooplankton taxa, and (2) the control of biodiversity and biocomplexity, for example, in the tropical ocean where diversity is high. These recommendations come from an assemblage of chemical, physical and biological oceanographers with experience in major interdisciplinary studies, including modeling. These recommendations are intended to stimulate efforts within the oceanographic community to facilitate the development of predictive capabilities for major biological processes in the ocean.

Full text

MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 222: 297–308, 2001 Published November 5
INTRODUCTION
Marine zooplankton function at many levels in ocean
food webs, as consumers, producers and prey. Ranging
in size from microns (protozooplankton) to centimeters
and meters (metazooplankton, including chains of
Thaliacea), they are also major contributors to elemen-
tal cycling and vertical fluxes. Despite more than
100 yr of research on these organisms, our knowledge
of their ecological function in their natural environ-
ment has increased only modestly. Presently we pos-
sess methods to quantify at least the abundances and
distributions of hard-bodied metazooplankton with
© Inter-Research 2001
*Participating scientists: U. Bathmann, M. H. Bundy, M. E.
Clarke, T. J. Cowles, K. Daly, H. G. Dam, M. M. Dekshe-
nieks, P. L. Donaghay, D. M. Gibson, D. J. Gifford, B. W.
Hansen, D. K. Hartline, E. J. H. Head, E. E. Hofmann, R. R.
Hopcroft, R. A. Jahnke, S. H. Jonasdottir, T. Kiørboe, G. S.
Kleppel, J. M. Klinck, P. M. Kremer, M. R. Landry, R. F. Lee,
P. H. Lenz, L. P. Madin, D. T. Manahan, M. G. Mazzocchi, D.
J. McGillicuddy, C. B. Miller, J. R. Nelson, T. R. Osborn,
G.-A. Paffenhöfer, R. E. Pieper, I. Prusova, M. R. Roman, S.
Schiel, H. E. Seim, S. L. Smith, J. J. Torres, P. G. Verity, S. G.
Wakeham, K. F. Wishner.
*Corresponding author: G.-A. Paffenhöfer, Skidaway Insti-
tute of Oceanography, 10 Ocean Science Circle, Savannah,
Georgia 31411, USA. E-mail: cmp@skio.peachnet.edu
THEME SECTION
Future marine zooplankton
research —a perspective
Marine Zooplankton Colloquium 2*
Georgia Coastal Center for Education, Savannah, Georgia 31401, USA
8–10 February 1999
ABSTRACT: During the Second Marine Zooplankton Colloquium (MZC2) 3 issues were added to
those developed 11 yr ago during the First Marine Zooplankton Colloquium (MZC1). First, we
focused on hot spots, i.e., locations where zooplankton occur in higher than regular abundance
and/or operate at higher rates. We should be able to determine the processes leading to such aggre-
gations and rates, and quantify their persistence. Second, information on the level of individual spe-
cies, even of highly abundant ones, is limited. Concerted efforts should be undertaken with highly
abundant to dominant species or genera (e.g., Oithona spp., Calanus spp., Oikopleura spp., Euphau-
sia superba) to determine what governs their abundance and its variability. Third, zooplankton
clearly influence biogeochemical cycling in the ocean, but our knowledge of the underlying pro-
cesses remains fragmentary. Therefore a thorough assessment of variables that still need to be quan-
tified is required to obtain an understanding of zooplankton contributions to biogeochemical cycling.
Combining studies on the 7 issues from MZC1 with the 3 from MZC2 should eventually lead to a
comprehensive understanding of (1) the mechanisms governing the abundance and existence of
dominant zooplankton taxa, and (2) the control of biodiversity and biocomplexity, for example, in the
tropical ocean where diversity is high. These recommendations come from an assemblage of chemi-
cal, physical and biological oceanographers with experience in major interdisciplinary studies,
including modeling. These recommendations are intended to stimulate efforts within the oceano-
graphic community to facilitate the development of predictive capabilities for major biological pro-
cesses in the ocean.
KEY WORDS: Marine zooplankton · Significant research issues
Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 222: 297– 308, 2001
accuracy, but have only coarse measures, acoustics for
example, to locate dense aggregations and determine
their temporal changes/variability. For neither proto-
zoa nor metazooplankton have we definitive methods
to determine key rates in situ, and most of the former
remain inaccessible to study at the species level.
Therefore it is not so much a lack of ideas but inade-
quate methodologies and instrumentation that limits
the pace of advances in understanding marine zoo-
plankton. Our ability to predict abundances and distri-
butions, even of the most studied species, is still at an
early stage. That realization resulted in the first Marine
Zooplankton Colloquium (MZC1) in April 1988 and led
to a second Marine Zooplankton Colloquium (MZC2)
in February 1999. Several of the participants of MZC1,
after consultations with colleagues, decided to orga-
nize MZC2, which addressed the following questions:
(1)Which major issues have emerged as additional crit-
ical topics during the past decade in our field? (2) How
can these issues be studied?
In the sections below, we first briefly consider the
progress made on research issues initially raised in
MZC1 (1989). While these issues remain significant for
now and the near future, the bulk of this report focuses
on 3 additional challenges that emerged in discussions
at MZC2.
PREVIOUS ISSUES
The 7 research issues of MZC1 are listed in Table 1,
each with several citations reflecting progress in that
area over the past 12 yr. Neither the references
selected for the table nor the brief comments below are
meant to be complete. They are only meant to illustrate
some of the ways in which advances have been real-
ized. A definitive evaluation of recent progress in
marine zooplankton ecology, requiring a more inten-
sive review of all 7 issues, would be an appropriate
way to mark the 20th anniversary of MZC1 in 2008.
Issue 1 (small-scale behaviors of individual zoo-
plankters) was stimulated by our lack of understanding
about how individual zooplankters behave and inter-
act with other organisms at scales of relevance in their
natural environment. Our citations of progress include
in situ observations as well as experimental studies
298
Issue Observation Source
(1) Small-scale In situ characterization of behavior of 9 copepod species Kimoto et al. (1988)
behavior of Behavior of ciliates to various stimuli Buskey & Stoecker (1989)
individual In situ behavior of Dioithona oculata Ambler et al. (1991)
zooplankters In situ preying of herring juveniles on Acartia Kils (1992)
Mate location of copepods Doall et al. (1998)
(2) Effects of environ- In situ indirect effects of invertebrate predators on copepods Neill (1990)
mental variability on In situ indirect effects of predatory fish on copepods Bollens & Frost (1991)
individual physiology Distribution of planktonic ciliates is affected by physical variables James & Hall (1995)
and behavior
(3) Relation of growth, Growth and reproduction of adult and juvenile copepods in situ Peterson et al. (1991)
fecundity and Fecundity etc. of Oithona davisae in relation to hydrographic variables Uye & Sano (1995)
mortality to In situ mortality of Centropages abdominalis Liang et al. (1996)
environmental Copepod egg production in relation to seston composition Jonasdottir et al. (1995)
conditions, past Changes in in situ copepod reproduction (3 mo) Niehoff et al. (1999)
and present Seasonal mortality of Oithona Nielsen et al. (1999)
(4) Definition Feeding on heterotrophs is seen as enhancing copepod condition Kleppel (1993)
of nutritional Food quality and quantity affect growth rates of ciliates Mischke (1994)
requirements Calanoid copepods prefer heterotrophs as food over diatoms Fessenden & Cowles (1994)
Copepod reproduction varies with the phytoplankton taxon eaten Ban et al. (1997)
Aldehydes from diatoms affect copepod egg viability negatively Miralto et al. (1999)
Aldehydes are produced by diatoms upon breakage Pohnert (2000)
(5) Long-term observa- Parallel trends of abundance of phytoplankton, zooplankton, and herring over 30 yr Aebischer et al. (1990)
tions of population and Ocean temperature increase is accompanied by zooplankton decline Roemmich & McGowan (1995)
community dynamics Decrease in fish stocks results in zooplankton increase (45 yr) Verheye et al. (1998)
and variability Daily variability of copepod in situ feeding over 3 mo Irigoien et al. (1998)
(6) Significance of Living species are identified by specific motion and live morphology Paffenhofer et al. (1996)
species Automated image recognition by the VPR and new algorithms Tang et al. (1998)
identification Closely related species can be distinguished with molecular technology Lindeque et al. (1999)
(7) Biological-physical Distribution of cod and haddock juveniles Werner et al. (1993)
model Three-dimensional biological-physical model Moisan et al. (1996)
development General overview of progress Hofmann & Lascara (1998)
Mechanisms of zooplankton behavior—species specific Carlotti & Wolf (1998)
Coupling of individual-based population dynamics model to a circulation model Miller et al. (1998)
General overview of progress Carlotti et al. (2000)
Table 1. Issues from MZC 1: recent advances on these issues, and sources

Marine Zooplankton Colloquium 2: Future marine zooplankton research
(Table 1). Notable is the promising technology that
enables in situ behavioral observations of individual
copepods Acartia discaudata being preyed upon by
individual juvenile herring, moving obliquely upwards
as a school (Kils 1992).
Issue 2 (effects of environmental variability on indi-
vidual physiology and behavior) stemmed from several
studies suggesting that zooplankton behaviors respond
more to the magnitude of variance of the conditions
encountered, rather than their average. Although this
issue has not received a major amount of research
attention, demonstrated behavioral responses include
the almost immediate response of Acartia hudsonica to
the introduction of predatory fish into enclosures (Bol-
lens & Frost 1991).
Issue 3 (relationship of growth, fecundity and mortal-
ity to environmental conditions, past and present) has
received considerable attention. For example, Peterson
et al. (1991) revealed how to obtain environmentally
realistic rates of growth and reproduction of copepods.
Obtaining comparable quantitative information on zoo-
plankton mortality rates continues to be a major stum-
bling block, but the approach by Ohman & Wood (1995)
is promising. A comprehensive field study in a stable
physical environment (e.g. with Calanus finmarchicus
as a likely predator of Oithona) could provide quantifi-
cation and some understanding of in situ mortality of a
major copepod genus (Nielsen et al. 1999).
Issue 4 (definition of nutritional requirements) was
addressed in a recent workshop (Kleppel 2001). We
emphasize here recent observations on the effects of
specific phytoplankton taxa on calanoid reproduction.
For example, aldehydes produced by 3 different spe-
cies of diatoms negatively affected calanoid egg viabil-
ity (Miralto et al. 1999, Pohnert 2000); however, other
phytoplankton may be nutritionally inadequate, rather
than toxic to zooplankton (e.g. Kleppel 1993, Jonas-
dottir et al. 1995).
Issue 5 (long-term observations of population and
community dynamics and variability) has been investi-
gated in several field studies. Aebischer et al. (1990)
showed the parallel trends of changes in the abun-
dance of phytoplankton, zooplankton and herring off
NE Great Britain over more than 30 yr, yet they stated
‘The mechanisms behind the parallelism in trends
remain unclear.’ This paper and Roemmich & Mc-
Gowan (1995) illustrate the value of long-term observa-
tions. Major efforts and investments will be needed to
conduct meaningful continuous long-term observations
(B. W. Frost pers. comm., presenting Brodeur et al.
1998).
Issue 6 (significance of species identification) is pro-
gressing with the advent of new technology and data
processing capability. Tang et al. (1998) showed indi-
rectly that automated zooplankton species identifica-
tion may be wishful thinking for the near future, espe-
cially when many similar species co-occur. However,
using motion and the morphology of appendages can
make it quite easy to separate even closely related spe-
cies, if observations are made on living animals (Paf-
fenhöfer et al. 1996). Taxonomic issues relating to open-
ocean forms of marine protists was not explicitly noted
in the MZC1 report but may ultimately be resolvable
with the broader application of molecular methods.
Issue 7 (biological-physical model development) has
progressed well in the 12 yr since MZC1. Recent
reviews by Hofmann & Lascara (1998) and Carlotti et al.
(2000) point towards the future. Virtual reality visual-
ization methods are of particular significance when
modeling the motions and behaviors of zooplankton.
Model development will be addressed further below as
part of the new issues raised at MZC2.
299
Issues Needed steps
(1) Significance of zooplankton hot spots (1) Information on dimensions, longevity of and activities
in hot spots, and their variability; mechanisms resulting in
hot spots; significance of hot spots for communities;
methods to locate hot spots and observe them non-invasively
(2) Information on individual species (2) Quantifications on 3 levels (integrative): (i) environment
and population; (ii) organism, its life history, activities,
bioenergetics; (iii) on molecular levels biochemical
adaptation and genetics. Utilize biological-physical
modeling for Issues (1) and (2), including advanced data
assimilation methods, circulation-biological models,
species-specific and nested models
(3) Zooplankton and biogeochemical cycles (3) Use new biomarkers to determine the fate of organic
matter; determine mechanisms of DOC production, and its
composition from various producers; develop nested
models with strong empirical input to understand
biogeochemical cycles in relation to food web interactions
Table 2. MZC2: issues and steps to accomplish them

Mar Ecol Prog Ser 222: 297– 308, 2001
NEW ISSUES
Of the 3 new issues identified at
MZC2, the first relates to zooplankton
hot spots, which in this context are
defined as volumes of water charac-
terized by enhanced biological activity
and/or concentrations of zooplankton.
Zooplankton hot spots are often domi-
nated by 1 or only a few species as,
for example, the dominance of zoo-
plankton biomass and part of the
food-web interactions by the copepod
Calanoides carinatus during the Ara-
bian Sea SW Monsoon (Smith et al.
1998). In order to unravel the func-
tional repertoires and food-web influ-
ences of such dominant species, con-
certed efforts are needed at the species
level, our second issue, ranging across
different length and time scales. Bio-
geochemical cycling by zooplankton,
including protozooplankton, is our
third issue. It has been inadequately addressed in
highly productive regions such as ocean margins.
Efforts have been made to consider the bulk biomass
and grazing properties of zooplankton in major JGOFS
studies; however, the main roles and contributions of
key dominant species have in most cases received
inadequate attention. Therefore, the mechanisms of
the contribution of abundant zooplankton species to
biogeochemical cycling could not be reliably deter-
mined.
Zooplankton hot spots
For the purpose of this discussion, zooplankton hot
spots are defined as ocean sites at which there is a recur-
rently pronounced zooplankton biomass signal and/or a
critical rate process, with biomass or rate parameters well
above the background mean. There is an implicit as-
sumption of higher activity, although biomass is usually the
signal. For example, an aggregation of inactive (diapaus-
ing) or senescent animals might not be considered a zoo-
plankton hot spot per se, but could be an area of enhanced
predatory activity. Often, high biomasses and/or rates are
found at physical discontinuities or associated with
episodic physical or environmental events, such as inter-
mittent upwellings (e.g. Paffenhöfer et al. 1987). To be a
zooplankton hot spot, a feature must be spatially identifi-
able over a significant period of time, and this may occur at
several scales simultaneously. Mackas et al. (1985) pro-
vided examples of spatial relationships and longevities of
phyto- and zooplankton patches related to physical
oceanographic processes. Zooplankton hot spots may be
present in shallow or deep water, nearshore or offshore.
Zooplankton aggregations as locations of hot spots
Zooplankton aggregations can occur on scales from
mm to near 100 km (Fig. 1). Among the smallest hot spots
are layers of heterotrophic flagellates moving continu-
ously around a dead copepod nauplius (G.-A.P. pers.
obs.). On a different scale, protozoa (Noctiluca miliaris)
can form feeding webs that last for months (Omori &
Hamner 1982). In Kiel Bight, a dense 30 cm layer of 100
000 cells ml–1of the tintinnid Stenosomella sp. was ob-
served with in situ instrumentation (Kils 1990). Eventu-
ally, it was located by a school of juvenile herring and
eaten within 25 min. Copepod aggregations occur over a
wide range of dimensions and periods of time (Fig. 1).
Salps and doliolids can develop into patches extending
over more than 100 km (Paffenhöfer et al. 1987).
Scyphomedusae can form swarms from several 100 m to
more than 10 km lasting from 1 d to >1 wk (Omori &
Hamner 1982, G.-A.P. pers. obs.).
Characterization and study of zooplankton hot spots
Specific questions and examples related to zoo-
plankton hot spots include the following:
(1) What is the spatial extent, longevity, and vari-
ability of a hot spot with regard to individual species
abundance or community organization? Although some
300
Fig. 1. Dimensions and longevity of aggregations of zooplankton. Data are from
Cushing & Tungate (1963), Omori & Hamner (1982), Ueda et al. (1985), Paffen-
höfer et al. (1987), Kimoto et al. (1988), Kils (1990), Ambler et al. (1991), Wish-
ner et al. (1995), Holliday et al. (1998), and G.-A.P. (pers. comm.)

Marine Zooplankton Colloquium 2: Future marine zooplankton research
information on spatial extent and longevity exists
(Fig. 1), the results are over-generalized. Recent ad-
vances in instrumentation and deployment techniques
have led to the discovery of thin layers of phytoplankton
and zooplankton ranging in thickness from a few tens of
cm to a few m, extending horizontally for several km and
persisting for >24 h (Hanson & Donaghay 1998, Holliday
et al. 1998). Changes in temporal and spatial environ-
mental features lead to variability in abundance, distrib-
ution and activity of zooplankton (MZC1 Issue 2). The
extent of those features will be of special interest in
attempting to understand the formation of zooplankton
hot spots.
(2) What are the mechanisms that lead to the for-
mation, maintenance and dispersion of zooplankton hot
spots? For example, Price (1989) demonstrated that many
specimens of the euphausiid Thysanoessa raschii
returned to feed on a patch of phytoplankton (i.e. the
phytoplankton provided a signal which resulted in the
aggregation of the euphausiid). Reproduction responses
to enhanced food can also provide a mechanism of patch
formation, as illustrated by the calanoid copepod Temora
turbinata in a phytoplankton-rich mass of upwelled
water (Paffenhöfer et al. 1987). Calanoid copepods prefer
strata of high primary productivity to those of high-
chlorophyll concentrations (Herman et al. 1981). Thus,
food quality may to be more important than quantity
(Kleppel 1993).
(3) Are zooplankton hot spots optimal habitats for some
species of zooplankton and/or their predators? The study
of Herman et al. (1981) seems to indicate that Calanus
and other copepods can choose vertically the most favor-
able location. Are such hot spots indicators of optimal
habitat for other kinds of species (i.e. fish that prey on the
zooplankton)? For example, during the SCOPEX project,
right whales migrated to the Cape Cod region each
spring, apparently in need of finding and feeding upon
very high concentrations of older life stages of a particular
copepod species Calanus finmarchicus in order to sustain
themselves (Wishner et al. 1995). The occurrence and
specific locations of suitable zooplankton swarms and
patches is a function of currents, weather, and water tem-
perature.
(4) What are the impacts of zooplankton hot spots on
individual species, including their life history strategies,
behavior and physiology? A hot spot driven by food may
only last as long as food is available (Price 1989). An indi-
vidual copepod species may occupy different depth lay-
ers as it grows from early nauplius to adulthood (e.g.
Miller 1993).
(5) What are the impacts of zooplankton hot spots on
communities, including fisheries, biogeochemical cycles,
and ecosystem function? Recruitment success of marine
fish stocks is in part related to conditions where food con-
centrations exceed mean levels (e.g. Lasker 1975).
Addressing the issue of zooplankton hot spots
There are 3 major challenges related to observing
and understanding the dynamics of zooplankton hot
spots: finding, sampling/observing and modeling. The
latter will be discussed in the following section on spe-
cies-level issues. Finding a hot spot requires (1) knowl-
edge of the physics and biology of the area to focus on
a likely location, (2) the use of remote sensing tools,
such as satellites, airplanes, and acoustic moorings, to
monitor the area and detect an event or feature, and
(3) specialized targeted sampling, such as fine-scale
(cm) vertical profiles once the probable location has
been identified.
Once found, the zooplankton hot spot needs to be
studied with adaptive sampling, relative to the feature it-
self and its spatial and temporal development. Continu-
ous studies over time are essential. Intermittent obser-
vations, such as one site visit per week or month, usually
do not provide sufficient data on magnitude and longe-
vity of in situ processes in dynamic regions. Rapid re-
sponse is needed for temporally ephemeral events. It is
vital to simultaneously quantify multiple variables of
physics, chemistry, and biology with real-time visual-
ization of data. Studies of rate processes and behavior,
which require greater amounts of time to undertake,
should be embedded within any synoptic program, but
this may sometimes require a different sampling plat-
form. Smaller-scale hot spots lasting seconds to minutes
over centimeters to meters can be observed with non-
invasive equipment, as shown by Kils (1992) using his
ecoSCOPE. Long Term Ecosystem Research (LTER)-type
efforts will be needed to determine the frequencies, du-
ration, and rates of larger-scale hot spots. Larger-scale
investigations are likely to be most successful in regions
of simple physical circulation and predictable zoo-
plankton assemblages; at the same time we need to
strive to develop means to quantify activities on scales of
basins. Continuous observations that combine both
acoustical (Holliday et al. 1998) and optical measure-
ments promise to provide valuable insights into taxon-
specific and stage-specific positioning and aggregations
(also MZC1 Issues 5 and 6). Our ability to understand
how zooplankton actually function will depend to a large
degree on technological advances in detecting identifi-
able targets at ecologically relevant scales.
The potential importance of zooplankton hot spots
had been suggested previously by Haury et al. (1978).
What is new is the availability of improved instrumen-
tation and methodology for studying these features at
the required spatial and temporal scales. Also, there is
a greater appreciation of the potential importance of
these hot spots, not merely as unique and interest-
ing phenomena but as major contributors to total-
ecosystem structure and function. Zooplankton hot
301

Mar Ecol Prog Ser 222: 297– 308, 2001
spots are critical to biogeochemical coupling, since
much of the material flux may occur at very specific
times and locations.
Species level
Within the context of a species-level focus 2 goals are
essential to the future research on marine zooplankton:
(1) understanding biodiversity and mechanisms of bio-
logical interactions, and (2) developing predictive
modeling capability. The first goal is oriented towards
curiosity-driven basic science. The second goal re-
quires a research agenda facilitating appropriate envi-
ronmental and biological data sets for models.
The working group recommended an integrative
and concerted approach that includes multiple levels
of biological analyses, from large-scale environments
and populations to cellular and molecular levels
(Fig. 2). The intent is to generate an understanding of a
particular species and the associated relevant pro-
cesses over a wide range of space and time scales. The
initial effort in marine zooplankton towards an under-
standing of function at the species level was made by
Marshall & Orr (1972), who dedicated their scientific
careers to studies of the copepod Calanus finmar-
chicus.
Characterization and study of the species-level
approach
At the level of the chemical, physical and biological
environment and specific populations, the integrative
approach focuses on ecology which includes patterns
and dispersal, and evolution, including adaptation and
genetic population structure, of a marine zooplankton
species (Fig. 2). At the next level, individual organ-
isms, the focus is on life histories, overwintering strate-
gies, various behaviors including mating, predator
avoidance and migrations, functional morphology
including motion and feeding, and bioenergetics such
as nutritional requirements and metabolic expendi-
tures. At the cellular and molecular levels biochemical
adaptations involving enzymes, and their genetic
bases, are of major interest. The species-specific
approach would provide an in-depth understanding
for a limited number of marine zooplankton species to
serve as a framework for considering ecosystem-level
processes. Individual species are the basic evolution-
ary unit in the marine biota, and a species-level
approach is an effective tool for studying organism-
environment interactions, as already considered in
MZC1 (i.e. characterization of individual small-scale
behaviors). This approach combines laboratory work
and fieldwork to address basic science questions and
to produce quantitative information for use in models
based on realistic biology.
To follow this recommendation, the focus in future
studies may be limited to one or a few abundant to
dominant species in a particular region, pelagic com-
munity or ecosystem. A comprehensive understanding
of a zooplankton species’ existence can only be accom-
plished if those parameters (including other zooplank-
ton taxa) affecting the species, and being affected by
the respective species, are included in the assess-
ments.
Another rationale for studying particular zooplank-
ton species comes from their part in regulating biogeo-
chemical cycling, biomass, and species diversity of
marine ecosystems. Zooplankton are a major link in
marine food webs and integral to nutrient and carbon
cycling. For example, protozooplankton and small-size
metazoans (small species and developmental stages)
contribute greatly to biogeochemical fluxes in epi-
pelagic waters over a wide latitudinal range. Small
302
Fig. 2. Integration of species-level studies through 3 levels:
population, organism, and cellular/molecular

Marine Zooplankton Colloquium 2: Future marine zooplankton research
metazooplankton taxa (e.g. Oithona,Oncaea and small
calanoids) can affect processes underlying marine
ecosystem function because of their numerical or bio-
mass dominance and their critical role as intermedi-
aries between the classical and microbial food webs
(Gonzalez et al. 1994). Changes in marine ecosystems,
due to either natural or human-induced variability,
could be observed through changes in communities of
marine zooplankton, including composition, diversity
and abundance.
Zooplankton taxa of significance
Examples of marine zooplankton taxa that could be
considered for study include the copepod Calanus fin-
marchicus, a dominant species in part of the North
Atlantic, and Calanoides carinatus from the northwest-
ern Indian Ocean and ocean margins of Africa. The
TransAtlantic Study of Calanus finmarchicus (TASC)
was an initial effort in an attempt to perform a species-
level study, as was the Subarctic Pacific Ecosystem
Research (SUPER) study, which focused mainly on 3
species of the genus Neocalanus (Miller 1993).
The small copepod genus Oithona occurs ubiqui-
tously and abundantly in the sea, from estuaries to the
open ocean and from tropical to polar regions (e.g. Paf-
fenhöfer 1993, Nielsen & Sabatini 1996). In the South-
ern Ocean production of O. similis may be higher than
each of the other zooplankton species there (Fransz &
Gonzalez 1995). The small copepod genus Oncaea,
which is ubiquitous except in estuaries, can be as
abundant as Oithona, and at times the dominant zoo-
plankton taxon (e.g. Antarctic waters, Metz 1998). The
potential significance of such small copepod genera in
the oceans’ pelagic communities and biogeochemical
cycles has only been recognized during the past sev-
eral years, because these organisms had not been col-
lected quantitatively earlier due to the use of coarse
net meshes.
The appendicularian genus Oikopleura is also
broadly distributed and is characterized by extraordi-
nary growth rates and short generation times (Deibel
1998, Hopcroft et al. 1998). The salp Thalia democrat-
ica occurs circumglobally in neritic subtropical waters
and is known for the fastest growth rates of any meta-
zoan (Heron 1972). Larger Salpa spp. can also occur in
high abundance and produce large, fast-sinking faecal
pellets. The euphausiid Euphausia superba is the dom-
inant metazooplankton species in the Antarctic Ocean
(e.g. Hopkins 1985), but its interannual variability is
large and alternates with high abundances of salps S.
thompsoni depending on ice cover. Oligotrich ciliates
such as the genus Strombidium and other genera con-
sume numerous species of nanoflagellates, which, in
turn, are major consumers of primary production and
bacterial secondary production.
Suitable study subjects are not limited to these
examples. Selection of ‘target’ species should certainly
require that they be major players in a significant
ecosystem. Beyond that, rewarding target species are
those that permit an integrative study through many
levels of analysis from evolutionary ecology to molecu-
lar biology. Therefore, other criteria might include
amenability to culture and information presently avail-
able in the literature.
Model development
Development and application of suitable models
should play a significant part in the future species-level
and hot spot studies. A recent workshop (US GLOBEC
1994) specifically recommended the following types of
marine zooplankton models: (1) models based on the
mechanisms that underlie animal behavior; (2) nested
models that allow transfer of information between indi-
viduals and populations; and (3) detailed mechanistic
models for a limited number of species. These sugges-
tions include a large part of the integrated research
suggested earlier in this section but also aspects related
to zooplankton hot spots. Advances in the modeling of
MZC1 Issue 1 have been made during the past 11 yr.
For example, some individual-based models include
small-scale behavior (Metridia lucens;Batchelder &
Williams 1995). Usually the behavior of zooplankton in
models is in the form of simple swimming and/or migra-
tion responses to changes in environmental conditions,
such as temperature, salinity or light (e.g. Dekshenieks
et al. 1996). Models that include parameterizations of
specific zooplankton motion behavior (e.g. drifting vs
directed swimming), specific feeding behavior (e.g.
feeding current vs attachment to particles vs swim-
ming) and their interactions are only now starting to be
developed. This direction in marine zooplankton mod-
eling requires detailed experimental observations sim-
ulating environmental conditions as closely as possible.
Since MZC1, there has been an emphasis on the
development of coupled physical-biological models
(Table 1: Hofmann & Lascara 1998, Carlotti et al. 2000).
Advances in ocean circulation modeling have resulted in
improved simulations of flow fields at nearly all scales.
Long-term predictability of physical variables has ad-
vanced (e.g. Griffies & Bryan 1997, Robinson et al. 1998),
as have data assimilation methods for biological and eco-
logical data (Lawson et al. 1995). To date, parameteriza-
tion of zooplankton in circulation-biological models is
usually in terms of average population characteristics for
functional groups (e.g. Fasham et al. 1990) and or spe-
cific species (e.g. Moisan et al. 1996, Miller et al. 1998).
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Mar Ecol Prog Ser 222: 297– 308, 2001
Future models will require not only improvements in the
representation of physics but also species-specific per-
formances of the respective abundant zooplankton gen-
era/species. Nested models that include parameteriza-
tions of individual and population processes have not
been developed. They will require better field and
experimental measuring capability, and advances in
computer resources.
Any environmentally oriented species-level model
will have to be interdisciplinary. Species-level models
and hot spot models both occur in an environment
affected by physical variables and numerous biological
and chemical parameters, usually including several
other zooplankton species as well, because no pelagic
environment exists where one zooplankton species is
exclusively abundant.
Zooplankton and biogeochemical cycles
Zooplankton directly affect the elemental stoichiom-
etry and material fluxes between particulate and dis-
solved matter through various processes associated
with the selective consumption and subsequent pro-
cessing of their food resources. The most widely recog-
nized link to biogeochemical fluxes is the repackaging
of digestive by-products into fast sinking fecal pellets
by relatively large animals (Noji 1991). Given the full
spectrum of pelagic consumers (including protists) and
the extent of their interactions within food webs, how-
ever, this is by no means the only way in which zoo-
plankton can regulate the efficiency of the biological
carbon pump or influence elemental cycles.
In the subsections below, we briefly consider the
implications of zooplankton-mediated processes in
modifying sinking particulate fluxes, in recycling and
distributing inorganic and organic materials through-
out the water column, and in determining the complex
dynamics of food-web structure and trophic flows.
Implicit in this discussion is a necessary progression of
approaches that might begin with simple theory and
experimental studies in bottles, but must extend to
measurable phenomena in natural settings and sys-
tem-level coupled models.
Modification of the downward POM flux
To achieve a mechanistic understanding of the de-
crease in particulate organic fluxes with depth, both
within and below the euphotic zone, we need to know to
what extent this decrease is due to the activities of zoo-
plankton versus other consumers such as bacteria (Banse
1990) or physical/chemical processes. Furthermore, we
need to know the rates and selectivities of zooplankton
in modifying the chemical makeup of sinking particulate
organic matter (POM) (Wakeham & Lee 1993). Since
most of the downward POM flux is in the form of rela-
tively large particulates (fecal pellets and aggregates;
Fowler & Knauer 1986), future research must also ad-
dress how zooplankton find and colonize such particles
and how fast they consume them (Kiørboe 2000). First,
however, we ought to find out which proto- and meta-
zooplankton taxa are the main colonizers and feeders.
Since grazing processes can also stimulate the metabolic
activity of bacteria, and in turn the microbial role in par-
ticle disaggregation, this is an area of research that po-
tentially involves synergistic influences of micro- and
macro-consumers that are no less complicated than food-
web interactions in the epipelagic zone.
One exciting possibility for investigating how zoo-
plankton modify the quality of the sinking POM is
the use of biomarkers to distinguish organic matter
sources and alteration processes (e.g. Brasell 1993,
Wakeham & Lee 1993). Progress in this area is
presently limited, however, by the relative scarcity of
unique biomarkers for phytoplankton prey, notable
exceptions being dinosterol for dinoflagellates and
long-chain alkenones for certain haptophytes (Brassell
1993). There are, however, virtually no biomarkers for
zooplankton. The situation is further complicated by
rapid digestive and biosynthetic alteration of dietary
organic matter by the zooplankton themselves, as well
as their assemblages of gut flora. Consequently, zoo-
plankton nutritional physiologists need to collaborate
closely with organic biogeochemists and microbiolo-
gists in developing useful new biomarkers for studying
the fate of organic matter.
Numerous previous studies have focused on the role of
zooplankton feeding on the packaging and vertical flux
of particulate organic materials (Noji 1991, Feinberg &
Dam 1998). Much less effort has been directed at exam-
ining the impacts of zooplankton on the recycling of bio-
genic materials in the upper water column. By influenc-
ing the efficiency of recycling, zooplankton plays a
critical role in determining the rate of regenerated pro-
duction. This provides a direct linkage between zoo-
plankton, primary production, and biogeochemical
cycles. Thus, future studies should place greater em-
phasis on the mechanisms and processes by which
zooplankton recycle nutrients and organic matter.
Dissolved inorganic and organic matter (DIM and
DOM): recycling and export
A multi-level protistan grazing chain is the dominant
trophic pathway in most open-ocean food webs, its
length ensuring that primary production will largely be
recycled rather than transferred to larger animals or
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Marine Zooplankton Colloquium 2: Future marine zooplankton research
exported. Although less important in absolute rates of
material cycling, larger animals have the unique abil-
ity, in such deep-water systems, to deposit their meta-
bolic by-products several hundreds of meters deeper
than their food source in the euphotic zone. In addition,
the active flux of both inorganic and organic carbon
and nitrogen due to diel vertical migrators and the
mortality of migrators below the pycnocline can signif-
icantly increase the exported production (Longhurst et
al. 1989, Dam et al. 1995, Zhang & Dam 1997). Data on
this topic remain scarce, however. Further studies
along gradients of latitude and productivity, similar to
that of Ikeda (1985), are essential to establish global
generalizations of the role of migrator-mediated fluxes
of DIM and DOM.
A related realization is that zooplankton-generated
DOM may be as important as that of phytoplankton in
enhancing bacterial biomass and productivity (Hygum et
al. 1997, Strom et al. 1997). These observations suggest
several questions for future research: (1) What are the
roles of zooplankton in supporting the microbial loop,
and are they fundamentally different for protistan versus
metazoan consumers? (2) What is the relative impor-
tance of alternate mechanisms of DOC production by
zooplankton (e.g. excretion, sloppy feeding, fecal leach-
ing) in the economy of the sea? (3) Is the biochemical
composition of the DOC produced by zooplankton dif-
ferent from that produced from algal exudation, and if
so, what are the consequences for bacterial production?
Additionally, we need to understand in much greater
detail how direct grazing and the altered digestive
products of zooplankton influence specific elemental
cycles and greenhouse-relevant gases. Some chal-
lenges related to this topic include studies of zooplank-
ton gut and fecal pellets as a habitat for anaerobic pro-
cesses such as methanogenesis (Tilbrook & Karl 1995),
grazing influences on DMS production and transfor-
mations (Dacey & Wakeham 1986, Wolfe & Steinke
1996, Tang et al. 2000), and grazer control of the redox
states and bioavailability of trace elements (Barbeau &
Moffett 2000).
Community structure and food-web dynamics
Within the context of a broad trophic network that
varies in time and space, the interactions of producers
and consumers have profound consequences for the
biogeochemistry of the oceans. Differences in the cou-
pling of production and grazing processes give rise, for
instance, to large regional and seasonal variations in
the magnitudes of phytoplankton standing stocks
(blooms), nutrient utilization and recycling efficien-
cies, and export ratios. Two questions related to food-
web dynamics seem to be particularly important to a
mechanistic understanding of oceanic biogeochem-
istry: (1) What are the roles of grazing and predation in
controlling growth of populations and maintaining
ecosystem stability in the open ocean (e.g. Frost &
Franzen 1992, Landry et al. 1997)? (2) How should
food-web interactions be nested in models of biogeo-
chemical cycles (Legendre & Rassoulzadegan 1996,
Verity & Smetacek 1996)?
To answer question (1), we need experimental stud-
ies to validate and define the operational rules of
potentially important regulatory mechanisms (e.g.
Department of Energy 1994). For example, are lower
limits of microbial population abundances set directly
by protistan grazing thresholds, as assumed without
sound supporting evidence in most models (Strom et
al. 2000), indirectly by more complex cascading influ-
ences of higher-order consumers (Calbet & Landry
1999), or by mechanisms as yet unappreciated?
Related to this topic, we also must begin to understand
when environmental factors can lead to large abun-
dances of zooplankton with unique capabilities re-
garding phytoplankton control and export (e.g. salps,
see also species level and hot spots) or whose secreted
tests or shells can comprise significant geochemical
pools and fluxes (foraminifera, radiolaria, pteropods).
Empiricists need to work closely with modelers as rec-
ommended in US GLOBEC (1994). One of the main fric-
tions in such interactions involves the modeller’s desire
to reduce the problem to its simplest terms and the em-
piricist’s desire to reproduce detailed behaviors of rec-
ognizable organisms and ecosystems. Zooplanktologists
can contribute to modelling efforts by participating in the
selection of model variables and processes and by lend-
ing their expertise to parameterization. In addition to
challenging the modeller’s structures and parameter val-
ues, zooplankton ecologists ought to appreciate the mod-
eller’s need for appropriate data sets and experimental
results to validate key mechanisms as well as the sys-
tem’s natural dynamics.
CONCLUSIONS
The 3-day MZC2 was an interdisciplinary attempt to
evaluate which issues would be of significance in
future marine zooplankton studies. The 3 new issues
that emerged from discussions focused on (1) zoo-
plankton hot spots, (2) species-level interactions, and
(3) biogeochemical cycling. These 3 foci complement
the 7 issues addressed at MZC1 11 yr ago, which will
continue to be major issues in the decades to come.
This document is based on the urgent need to compre-
hend the function of biological processes in the ocean,
and to enhance the recent pace of progress. Future
major advances, not just in marine zooplankton re-
305

Mar Ecol Prog Ser 222: 297– 308, 2001
search but in biological oceanography sensu strictu
towards understanding community and eventually
ecosystem functioning, and its variability, will be a
function of setting priorities. We will not be able to
develop a solid predictive capability on the signifi-
cance of zooplankton in the pelagic environment, and
therefore a general understanding of its functioning,
until we can determine the mechanisms of the zoo-
plankton’s contribution (e.g. Aebischer et al. 1990).
Determining such mechanisms and developing predic-
tive capabilities depends on (1) continuous long-term
observations not just on abundant zooplankton taxa
but also of the major physical, chemical and biological
variables governing their occurrence, distribution and
abundance, (2) in situ rate quantifications of feeding,
growth, mortality etc., accompanying the long-term
observations, and (3) parallel interdisciplinary model-
ing (e.g. Hofmann & Lascara 1998, Carlotti et al. 2000).
Acknowledgements. This colloquium was made possible by
the commitment of more than 40 marine scientists who self-
lessly provided time and funds. The Skidaway Marine Sci-
ence Foundation under the direction of Carol Megathlin sup-
ported the colloquium financially. The Georgia Coastal
Center for Education provided meeting facilities. We grate-
fully acknowledge their support. This report was composed
using a framework established at the meeting and repeatedly
revised by several participants, who spent numerous hours to
improving it.
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308
Editorial responsibility: Otto Kinne (Editor),
Oldendorf/Luhe, Germany
Submitted: December 9, 2000; Accepted: August 2, 2001
Proofs received from author(s): October 17, 2001
Erratum Mar Ecol Prog Ser 218: 95 –106, 2001
Flow and particle distributions in a nearshore seagrass meadow before and after a storm
T. C. Granata1,*, T. Serra2, J. Colomer2, X. Casamitjana2, C. M. Duarte1,**, E. Gacia1, J. K. Petersen3
1Centre d’Estudis Avançats de Blanes, C. Santa Bàrbara s/n, 17300 Blanes (Girona), Spain
2Environmental Physics, Department of Physics, University of Girona, Campus de Montilivi, 17071 Girona, Spain
3National Environmental Research Institute, Frederiksborgvej 399, 4000 Roskilde, Denmark
• J. K. Petersen was accidentally omitted from the list of
authors. Also, the first author's e-mail address has been up-
dated. The corrected list of authors and their addresses is
given here.
Present addresses:
***Ecological Engineering Program, The Ohio State Univer-
sity, CEEGS 470 Hitchcock Hall 2070 Neil Avenue, Colum-
bus, Ohio 43210-1275, USA. E-mail: granata.6@osu.edu
***Instituto Mediterraneo de Estudios Avanzados, C. Vallde-
mossa km 7.5, 07071 Palma de Mallorca, Spain