6 Trophic interactions
It is impossible to discuss the fate of new production by diazotrophs without discussing trophic interactions. Colonies of Trichodesmium provide stable “homes” for a numerous and diverse association of organisms (Siddiqui et al., 1992; Sellner, 1997; O’Neil, 1999; Sheridan et al., 2002). This creates a complex microenvironment with multifarious pathways for internal nutrient cycling. Sheridan et al. (2002) estimated that 85% of Trichodesmium colonies were inhabited by other organisms. Colonizing organisms include bacteria, other cyanobacteria, fungi, pennate and centric diatoms, heterotrophic and autotrophic dinoflagellates, chrysophytes, ciliates, amoebae, hydroids, different life stages of harpacticoid copepods and juvenile decapods. Bacteria and dinoflagellates were the most common associates (Sheridan et al., 2002). Despite the fact that colonies are rich microenvironments, there is a variety of evidence suggesting that Trichodesmium themselves go largely ungrazed (see below) and so viral cell lysis and decomposition are the likely fates for many of these populations (nutrient accumulation), and that the importance of higher trophic levels in processing Trichodesmium biomass is minimal as compared to recycled primary production and bacterial productivity. Consistent with this idea is the observation that a variety of phytoplankton, bacteria, and higher trophic levels cooccur or occur in the water column subsequent to blooms of Trichodesmium spp. (Devassy, 1978, 1979; Revelante et al., 1982; Furnas and Mitchell, 1996; Walsh and Steidinger, 2001; Mulholland et al., 2006). It is thought that these communities are relieved from N limitation as a result of N release from Trichodesmium.
Trichodesmium occur as variously sized and shaped aggregates or colonies but also as free filaments or trichomes. Large colonies may contain hundreds of trichomes. However, the average colony size and colony abundance can vary from day to day (Devassy et al., 1978). Colonies take the form of bundles with trichomes arranged in parallel (tufts) or radially (puffs). Little is known about the causes of bundle formation, but the distributions of free filaments and bundles vary regionally and apparently with the degree of turbulence (Bryceson and Fay, 1981; Mahaffey et al., 2005). The purpose of bundle formation is also unclear, but there has been speculation that it may be a behavioral strategy for minimizing the exposure of nitrogenase (an oxygen sensitive protein) to oxygen (e.g., Paerl et al., 1989; Gallon, 1992). Regardless of the reasons colonies form, the trophodynamics of Trichodesmium vary depending on morphology, the amount of stable surface area, and interfilamental space available for colonization.
There are few direct measurements of the trophic transfer of recently fixed N or C through Trichodesmium. Bryceson and Fay (1981) first demonstrated that the trophic transfer of recently fixed N2 might be important in communities dominated by Trichodesmium and they subsequently demonstrated isotopic enrichment in non-Trichodesmium size fractions after incubation of Trichodesmium and natural marine communities with 15N2. They did not have control incubations to account for N2 fixation by smaller diazotrophic cyanobacteria and bacterioplankton but, nevertheless, they report enrichment in the 2 to 30μm and 0.2 to 2.0μm size fractions (Bryceson and Fay, 1981). Subsequently, the only other direct estimates of the trophic transfer of recently fixed N2 demonstrated that up to 11% of recently fixed N2 was transferred to non-N2 fixing cells in whole water samples even in short (2 h) incubations (Mulholland et al., 2004b). This suggests that Trichodesmium may support further productivity in the upper water column and the growth of cooccurring organisms, including heterotrophs, rather than a substantial direct particle sinking flux (Fig. 1). Despite the idea that dissolved nutrients may be the primary route of trophic transfer of recently fixed N2, isotopically “light” zooplankton have been collected from the tropical Atlantic (Montoya et al., 2002) and isotopically light sediment trap material was collected under a station experiencing a Trichodesmium bloom in the Indian Ocean (Capone et al., 1998). In addition, low 15N values have been reported in sediment trap material at both the Atlantic and Pacific time series sites (Karl et al., 1997, 2002; Knapp et al., 2005), indicating that recently fixed N2, which has an isotopic signature similar to atmospheric N, is being transferred to higher trophic levels and leaving the euphotic zone. In contrast, Brandes et al. (1998) suggested that material derived from N2 fixation could also be remineralized in the upper water column and hypothesized that the input of isotopically light N from N2 fixation was responsible for a lightening of the isotopic nitrate signal in surface waters above the oxygen minimum zone in the Arabian Sea. Based on excess N2 gas concentrations, Devol (2007) and Devol et al. (2006) have gone on to speculate that the particle rain from diazotrophic production fuels denitrification in the oxygen minimum zone there. These observations suggest that diazotrophic production can be remineralized in surface waters fueling microbial production and complicating interpretation of geochemical tracers such as stable isotope signatures and N*.
6.1 Bacteria
Bacterial associates with Trichodesmium colonies have been widely observed (Paerl et al., 1989; Nausch, 1996; Sheridan et al., 2002; Renaud et al., 2005; Mulholland et al., unpublished data). Trichodesmium colonies are inhabited by both rod-shaped and filamentous bacteria, as are many other filamentous cyanobacteria (Paerl et al., 1989). Bacterial associates also included heterotrophic N2 fixers, were located around and within aggregates where they took up carbohydrates and amino acids.
Varying degrees of enrichment of bacteria have been found on and around colonies. Nausch (1996) reported that bacteria were 2 to 5 times higher on colonies of Trichodesmium than in the surrounding water, however, during her study, Trichodesmium were not abundant, the water column was turbulent, and colonies were small. At BATS, Sheridan et al. (2002) report that bacteria were enriched on average 401 and 1709 times on Trichodesmium puffs and tufts, respectively. Carpenter and Price (1977) found that up to 8.3% of Trichodesmium were populated by bacteria in the Sargasso Sea. So, it appears that there is high variability in the degree of bacterial colonization of Trichodesmium aggregates. In terms of their productivity, Nausch (1996) found thymidine incorporation to be enhanced in association with colonies of Trichodesmium relative to that of the water column and comparable to the enrichment found in marine snow. However, because colony-associated bacterial abundance was so much higher, when normalized per unit bacteria, thymidine incorporation associated with colonies appeared to be lower than that measured in the surrounding water. In the Gulf of Mexico, leucine incorporation increased by up to 72% in association with Trichodesmium colonies relative to the surrounding water column (Mulholland et al., unpublished data). Similarly, Tseng et al. (2005) found that bacterial productivity and abundance were higher but productivity per unit bacterial biomass was lower, in association with Trichodesmium populations. In addition, they found that populations became more autotrophic during times of the year when Trichodesmium was abundant (lower bacterial productivity: primary productivity ratio). The authors attribute this to N release and alleviation of competition between bacteria and phytoplankton for scarce NH+4 . However, they also note that Trichodesmium occurred as free filaments in the Kuroshio and therefore lacked harpacticoid grazer populations and associated organisms observed in other communities (Tseng et al., 2005).
High rates of amino acid oxidase activity (Mulholland et al., 1998; Glibert and O’Neil 1999), peptide hydrolysis (Mulholland et al. unpublished data), and hydrolytic enzyme activity have also been found in association with Trichodesmium colonies, suggesting bacteria and other organisms (e.g., phytoplankton and grazers) associated with colonies actively cycle nutrients. Rates of enzyme activity in and around colonies in these studies were higher than those observed in the surrounding water column reflecting either more active or more abundant microbial communities. Nausch (1996) calculated C and N release rates between 30.5 and 1086 ng C col−1 h−1 and 4.6 to 209 ng N col−1 h−1, respectively, based on hydrolytic enzyme activities associated with Trichodesmium colonies.
6.2 Phytoplankton
In some coastal systems, blooms of dinoflagellates and diatoms have been observed during and subsequent to Trichodesmium blooms (Devassy et al., 1978; Revelante et al., 1982; Furnas and Mitchell, 1996). For example, Devassy et al. (1979) found that as blooms of Trichodesmium decayed, Chaetoceras populations increased, followed by a succession of cladocerans, dinoflagellates, green algae, copepods, and finally, carnivores. On the West Florida shelf, dense Karenia brevis blooms occur during and subsequent to Trichodesmium blooms and it has been hypothesized that they provide a source of new N to fuel destructive red tides (Walsh and Steidinger, 2001; Mulholland et al., 2006). Based on direct estimates of N2 fixation, N release, and in situ water column N uptake rates, Trichodesmium produced ample dissolved N to fuel K. brevis growth in the Gulf of Mexico (Mulholland et al., 2006).
Experiments suggest that Tetraselmis grew well on decaying Trichodesmium (Devassy et al., 1978). Similarly, Karenia brevis cultures grew well on culture medium enriched in Trichodesmium exudates as the sole source of nitrogen (Mulholland et al., unpublished data). Although direct evidence of trophic transfer from Trichodesmium to phytoplankton in nature is lacking, Bryceson and Fay (1981) and Mulholland et al. (2004b), demonstrated that 15N derived from 15N2 additions moved into the co-occurring plankton, which presumably included a variety of phytoplankton. Further, the low 15N observed in sediment trap material suggests that at least some N derived from diazotrophy is leaving the euphotic zone (Karl et al., 1997, 2002; Capone et al., 1998; Montoya et al., 2002; Knapp et al., 2005).
6.3 Zooplankton and higher trophic levels
The fate of recently fixed N2 and transfer of Trichodesmium biomass to higher trophic levels is poorly understood. Although a variety of herbivores are thought to graze on Trichodesmium (e.g., Sellner, 1997), Trichodesmium spp. are not grazed by many of the dominant zooplankton in marine systems and are toxic to many copepods (Hawser and Codd, 1992; O’Neil, 1999). Some specialized harpacticoid copepods do graze on and inhabit Trichodesmium colonies but these do not produce fecal pellets that would rapidly remove grazed material from the euphotic zone (O’Neil and Roman, 1994; O’Neil et al., 1996).
O’Neil et al. (1996) estimated that the harpacticoid copepod, Macrosetella, could consume 33–45% of total colony N, or 100% of the new N2 fixed each day. The copepod then excretes 48% of its body N per day, mainly as NH+4 , thereby recycling much of the N in the water column (O’Neil et al., 1996). Further, Roman (1978) found that Macrosetella could ingest from 90 to 126% of its body carbon per day when feeding on Trichodesmium. Based on stoichiometric arguments, O’Neil (1999) calculated 30% of the recently fixed C from Trichodesmium spp. flowed into grazers and because Macrosetella appears to have a higher C:N ratio than the Trichodesmium spp. themselves, they are likely to excrete excess N. Therefore, the major flux of recently fixed N and C through zooplankton may also be through extracellular release and dissolved nutrient pools. In addition to excretory release, zooplankton grazers can mediate the transfer of N through additional release from sloppy feeding (O’Neil and Roman, 1996).
Not much is known about higher trophic levels, although isotopic evidence suggests that there are other grazers of Trichodesmium (e.g., Montoya et al., 2002). In general, it has been observed that there is a low quality of fish associated with blooms, although Trichodesmium do not appear to be directly toxic to fish (Devassy et al., 1978). Fish and some other higher trophic levels have been observed to graze on Trichodesmium (see Carpenter and Capone, 2007).
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