The flow of Nitrogen through a Planktonic Foodweb
Jo Bayes 326575
Final grade: 95%
“In trophic webs, as in Escher paintings, flow can be upward or downward. From every
intermediate level in a trophic web there are ‘ladders’ going up and ‘chutes’ going down, and the
major players in the game are not restricted to the top or the bottom of the web.” (Hunter &
Price, 1992)
We have had this view of planktonic marine food webs since the 1980s when improvements in
technological methods led to more accurate collecting and measuring of microbial organisms,
such as bacteria, heterotrophic nanoflagellates (HNF), diatoms, dinoflagellates and ciliates. This
has given us a much better understanding of the complex interactions which are at the very base
of the marine food web and support much of the life in the oceans. The term used for these
microscopic interactions is ‘The Microbial Loop’. The main hurdle in understanding the
importance of the microbial loop was the underestimation of bacterial biomass (only about 10%
of the true in situ biomass had previously been recorded), this coupled with the fact that bacteria
are too small to be consumed by crustacean mesozooplankton led to the school of though that
bacteria had little to do with the aquatic food chain and were considered only to be decomposers
of detritus and particulate organic matter (POM). In fact the latter part of this statement is true
with detrital production of dissolved organic matter (DOM) and leakage from grazers being the
dominant sources of bacterial food (Jackson & Eldridge, 1992), however we now also know that
bacteria play a huge role in transferring particulate and dissolved organic nitrogen to protozoans
and into the aquatic food web.
Microbial loop organisms play a hugely important role in channelling energy from the
picoplankton up through trophic levels to larger metazoan plankton as well as organisms of the
nekton. However, it is important to note that this is not a simple linear chain and as noted by
Hunter & Price (1992) many organisms can fill a number of different trophic roles and interact
with each other in a number of different ways. Due to this added complexity it is important to
have a clear understanding of the classification of the trophic roles in the aquatic food web
(Mousseau et al., 2001).
Productivity in the oceans depends almost entirely on phytoplankton. Phytoplankton are
photoautotrophs, which form the base of aquatic food webs by converting radiant energy into
chemical energy by C-fixation. In temperate waters, such as those surrounding the Isle of
Cumbrae dinoflagellate (E.g. Ceratium spp) and diatom (E.g. Melosira sp., Skeletonema
costatum) blooms are important components of the aquatic food chain, however it has recently
been discovered that with the exception of these seasonal blooms, the majority of C-fixation in
the oceans is carried out by picoeukaryotes (photoautotrophs ranging in size from 0.2-2µm). In
order to photosynthesise phytoplankton need light, and must therefore live within the euphotic
zone, this generally limits them to the top 50-100m of the water column (Marshall & Orr, 1956).
In addition to sunlight photoautotrophic organisms also require nutrients, with the most common
growth-limiting nutrient in the marine environment being nitrogen. These two environmental
actors control algal biomass from the ‘bottom-up’, however phytoplankton populations are also
controlled from the ‘top-down’ through grazing activities of heterotrophic dinoflagellates,
ciliates and metazoan predators.
Over 50% of dinoflagellate species are known to be heterotrophic (Dinophysis acuta) and an
increasing number are being found to be mixotrophic (Ceratium fusus). Amongst the
heterotrophs there are three feeding mechanisms, these are (i) the ingestion of whole cells
(phagocytosis), this is used by Gyrodinium spirale which plays an important role as a predator
on other dinoflagellates, in particular those which cause red tides, (ii) The use of a peduncle as
seen by Dinophysis acuta, and (iii) the use of a pallium which is displayed in the feeding
behaviour of Protoperidinium spp. Heterotrophic dinoflagellates are remarkable in that they are
able to feed on prey of similar sizes to themselves, thus individuals larger than 20µm are able to
compete with copepods for prey. Also, as their generation time is similarly matched to that of
their phytoplankton prey they are able to respond faster to blooms thus keeping the nutrients,
including nitrogen, within the euphotic zone and making them available to higher trophic
organisms.
Ciliates, in particular those which have mixotrophic lifestyles, such as Mesodinium rubrum, are
another important group to consider when tracking the flow of nitrogen in the aquatic food web.
This is because they are both important grazers of HNF as well as forming a dominant
component of the total photosynthetic biomass in many marine environments. The obvious
advantage to a mixotrophic lifestyle is that when mixed out of the euphotic zone growth can be
sustained by switching to phagotrophy. This adaptation allows mixotrophic organisms to out
compete obligate photo- or heterotrophic organisms when limited by either light or particulate
food. They excrete nitrogen through heterotrophic processes, whilst simultaneously requiring
dissolved inorganic nitrogen (DIN) for their photosynthetic endosymbionts. The transfer of
nitrogen between host and symbiont is still not fully understood and it remains unknown whether
mixotrophic ciliates are net consumers or producers of nitrogen.
Metazoan predators include the crustacean zooplankton, namely copepods as well as the
planktonic larvae, which forms the meroplankton. Copepods, including Acartia clausi,
Centropages spp. and Temora longicornis, are the most dominant form of marine zooplankton,
forming 50-80% numerically of the group. They are important as grazers of phytoplankton
including toxic diatoms. The copepod Temora longicornis grazes on pennate diatoms and will
feed on both toxic and non-toxic species equally (Lincoln et al., 2001). Due to the fact that
T.longicornis falls prey to larger zooplankton and planktivorous fish it is important to monitor
the transmission of this toxin as it is possible that T. longicornis may facilitate its transmission to
higher trophic levels, leading to serious results for the marine ecosystem, maritime economy and
public health.There is further evidence from studies by Daan et al. (1981), which show that in
periods of low phytoplankton concentrations T. longicornis is also able to switch to cannibalism
as an alternative foraging strategy, selectively feeding on nauplii.
The organisms making up the meroplankton are mainly larval stages of crustaceans, including
decapod zoea and megalopa (e.g. Carcinus maenas), but also include polychaete larvae and
enchinoderm ophiopleutes and echinopleutes. During some seasons the meroplankton can
constitute more than 50% of the plankton biomass. These organisms therefore play a significant
role in filling the intermediate stage in many food webs, making energy from protozoa available
to large metazoan predators and nektonic organisms. However, large zooplankton both enhance
and reduce nitrogen flow; Firstly they release nitrogen as ammonium, urea and amino acids,
however as they also graze upon the primary consumers (phytoplankton) and regenerators
(protozoa) of nitrogen, the dynamics of their trophic interactions will result in either a net
positive or negative impact on the regeneration of nitrogen in the system.
With the different trophic roles now explained it is possible to look at the interactions between
the planktonic organisms collected from the Cylde sea and to follow the flow of nitrogen, in its
various forms through the planktonic food web in more detail.
As previously mentioned phytoplankton must acquire a range of substrates from their
environment in order to maintain growth and cellular division. Some of the universally required
elements are available in excess to requirement, for example sodium (Na+), magnesium (Mg2+),
calcium (Ca2+) and potassium (K+) ions as well as carbon dioxide. In addition to these freely
available constituents, phytoplankton also need a variety of elements, which are present only in
small amounts. The most important of these are nitrogen and phosphorous, which are crucial for
all phytoplankton as well as silica, which is required by diatoms in order to form their siliceous
frustules (e.g.Chaetoceros spp.). Nitrogen is distinguished from other elements for the wide
range of forms in which it occurs in seawater, reflecting the complexity of the chemistry of the
element and the nitrogen cycle (Raymont, 1980). The forms that have been detected in seawater
include molecular nitrogen (N2) and nitrous oxide (N2O) as dissolved gases, the ionic forms
nitrite (NO2-), nitrate (NO3-) and ammonium (NH4+), in addition to dissolved organic nitrogen
(DON), as urea and particulate organic forms (PON). These latter two forms can only be utilised
by bacteria and enter the microbial food web through them. DON and PON are formed however
with the sinking and incorporation of dead zooplankton, diatoms and crustacean moults to the
benthos.
The flux of inorganic nitrogen, namely as nitrate and ammonium, is however more complex than
the organic flux and the two forms have been classified as ‘new’ and ‘regenerated’ nitrogen
respectively. Dugdale & Goering first presented the distinction between ‘new and regenerated’
nitrogen in 1967, where new production is described as phytoplankton growth fuelled
predominantly by nitrate. It is supplied to the euphotic zone by surface run off, riverine input or
by turbulent mixing of water from below the thermocline. Regenerated production is the when
the majority of phytoplankton growth is fuelled by ammonium. Ammonium is remineralised
within the euphotic zone as a result of metabolism and excretion by zooplankton and bacteria.
In a marine food chain it is generally thought that phytoplankters are the main utilisers of
inorganic nitrogen, preferentially using ammonium, (this is due to the energetic advantages, as
ammonium can be directly used for the synthesis of amino acids, where as nitrate must be first
reduced using a series of endothermic reactions) whilst the micro- and macro-zooplankton are
thought to be the main remineralisers, there is also evidence that protozoa play a substantial part
in remineralisation. There are three important factors when considering the role of protozoans as
nitrogen assimilators or regenerators;
(i) Organism Size.
As the size of an organism increases the rate of nutrient excretion per unit of body weight
decreases (Caron & Goldmas, 1990). Thus the smaller protozoa play a more substantial role than
the larger metazoan zooplankton, and bacteria more so than protozoa.
(ii) Gross Growth Efficiency.
This is the percentage of ingested energy that is used by an organism to increase its cellular
mass. In general smaller organisms have higher gross growth efficiencies than larger organisms.
This means that for a given biomass a smaller organism will assimilate more nutrients than a
larger organism.
(iii) Food Quality. This is the key factor and is exclusive of organism size. It refers to the C:N
ratio of the organism. For example, if the prey organism has a higher C:N ratio compared to its
predator the nitrogen of the prey will be incorporated into the cellular mass of the consumer (an
example of this is copepods feeding on phytoplankton.However if they prey organism has a
lower C:N ratio than its predator, the excess nitrogen will be released in the remineralised for as
ammonium (this is seen when HNF feed upon bacteria, thus making HNF extremely important in
nitrogen regeneration.)
Although it is known that these organisms act as both nitrogen assimilators and regenerators our
knowledge on the subject is still incomplete as it is extremely difficult to measure regeneration
rates as, as soon as nitrogen is excreted it is effectively immediately taken up again.
It is evident from Figure 3.1 along with the description of the marine food web and the flow of
nitrogen through it that the system is highly complex, with numerous interactions. It is also
important for us to understand these interactions and improve our knowledge about these small
uni- and multi-celluar organisms, which the majority of our ocean life depends on. This matter is
even more urgent as anthropogenic activities continue to disrupt natural biogeochemical cycles
and in the last few decades it has been the nitrogen cycle, which has been most greatly affected.
Coastal seas in particular have been subject to increased productivity, which often leads to
nuisance, or toxic blooms having a detrimental effect on the surrounding environment (Stolte,
1996). In the face of climate change and increasing nutrient release through human activities it is
even more important that we fully understand the nitrogen cycle through the atmosphere, land
and oceans (Arrigo, 2005) and to do this we must be fully aware of the underlying microscopic
processes driving the cycle. This places even more importance on the quantitative studies of the
flux of nitrogen in marine planktonic food webs, as it is an area of investigation, which remains
problematic. However by tracing stable isotopes within organisms at different trophic levels it is
possible to measure whether organisms are predominantly utilisers or regenerators of nitrogen
within the system. Accurate estimates of rate processes will then allow the determination of
fluxes between trophic levels and can be used for the parameterisation of mathematical models
of microbial food webs (Davidson et al., 2005).