The present study is the first to reveal the existence of specific micro- and mesozooplankton communities exported from the reef tops of a shallow tropical reef ecosystem and the importance of neritic-estuarine copepod species for this environment.
The use of passive net systems adapted for zooplankton sampling at specific points in the reef environment, with a 64 μm mesh size, permitted the sampling design of the present study, that allowed the collection of reef-associated zooplankton and organisms transported in channels between reefs, as well as the evaluation of the carbon mass of zooplankton available as food source for higher trophic levels. The significant buildup of zooplankton at both reefs sites and all sampling nights indicates the existence of a hitherto unknown mechanism that enriches the zooplankton above emerging intertidal reef tops.
Zooplankton buildup at reefs—a hitherto neglected mechanism
The unexpectedly high abundances found at the reef edges point at the existence of a hitherto unknown mechanism. One part of this mechanism is the accumulation of zooplankton at the offshore side of reefs, which has been described by Genin et al. [38]. They described a situation where downwelling and upwelling driven by the interaction of currents and coastal topography generate zooplankton accumulations. In such downwelling and accumulation zones at the offshore reef edges, active zooplankters such as copepods actively maintain their vertical position in the water column, swimming upwards against the vertical flow. This may lead to huge accumulation rates at coastal frontal zones close to the offshore reef edges, constituting a well-documented aggregation and accumulation mechanism [38,39,40,41,42]. In our study area, high densities can be expected to occur at the windward offshore edges of the reefs, where there is consistent downwelling in coastal convergence fronts, mostly due to onshore winds.
In the present study, sampling could not be conducted at the windward (offshore) edge of the Tamandaré reefs, considering the year-round predominance of strong onshore trade winds in this area that lead to big waves and unsecure navigation conditions at the offshore edges of the reefs. Rather, sampling sites for the REN were chosen to receive the water washed from the emerging reef tops during ebb flow. High densities found at these sites are indicative of a hitherto unknown accumulation mechanism that acts according to the tidal cycle at new moon nights, from dusk to dawn. It consists in the following three steps (1) low tide: accumulation of zooplankton at the windward side of emerged reef tops due to the above mentioned processes, (2) flooding tide: coastal waters with high densities of zooplankton are sucked towards the submerging reefs at nocturnal low tides, (3) vertical habitat compression (i.e., decrease of available water column) above the emerging reef tops during ebb tide, (4) discharge of high-density zooplankton from emerging reef tops during ebb tides, towards the onshore reef edges.
Another important factor is that predation due to scleractinian corals is negligible in the study area, since corals are very rare and occur at a negligibly low cover on reef tops in the Tamandaré area (< 0.2%, [43]). Also, the Tamandaré reefs show very low densities of planktivores [44]. This overall low predation on zooplankton also contributes to the observed high abundances.
Conversely, many other studies showed a significant depletion of zooplankton at oligotrophic coral reef ecosystems, mainly due to intensive predation by benthic sessile planktivores (e.g., scleractinian corals). The high abundance at reef edges compared to the samples collected in open water channels thus represents an opposite pattern to the one found in many previous studies on micro- and mesozooplankton (mesh aperture between 40 and 125 μm) on coral reefs, where the lowest abundances of zooplankton were always found near the reefs [12, 19,20,21].
In contrast to the present study, Santos et al. [31] found no significant differences between CMNN and REN samples taken in the study area (regarding total wet biomass, total abundance, and length-frequency distributions), based on three sampling nights in November 2015. The apparent discrepancy between the Santos et al. [31] results and the present study can be well explained by differences in objectives, gear used, laboratory methods, and the considerably larger data set used in the present study. Santos et al. [31] presented and described the two new passive gears (REN and CMNN) in detail, and compared them with standard plankton net tows, based on a very small dataset (n = 3 sampling nights). While they used different mesh sizes, we used only 64 micron mesh nets to compare habitats, and unveiled a new community of micro- and mesozooplankton at the reef edges. Furthermore, the present study shows new results with a much larger dataset (n = 8 sampling nights, two gears, two areas, 8 * 2 * 2 = 32 samples). The Santos et al. [31] study used rapid semi-automatic laboratory methods (size distribution of large groups, no species), based on only one subsample per sample. We used detailed taxonomic identifications and determination of carbon mass, based on three subsamples per sample. The much larger dataset allowed us to detect striking, significant differences between reef edge and channel habitats, and to describe unexpectedly high abundances at the reef edges, especially in March 2016.
In most oligotrophic coral reefs, scleractinian cnidarians are considered voracious nocturnal predators of zooplankton [3, 45,46,47]. Due to this high predatory pressure near the bottom, organisms living on reefs with high coral cover show a marked vertical migration at night, i.e., where there is an evident zooplankton enrichment on the surface. The high cover of planktivorous sessile organisms, such as scleractinian corals, explained lower abundances near the reef than in adjacent open waters, in previous studies in such coral reefs [12, 19,20,21].
Yet, the coastal reefs of northeastern Brazil exhibit a very low coral cover [43, 48,49,50], probably due to the regular estuarine influx of freshwater, pollutants and sediments at peak rainy season (April to August) and during extreme flooding events [23, 25, 26]. The paucity of scleractinian corals leads to a low predatory pressure on zooplankton at the Tamandaré reef tops. Conversely, there is a rich algal cover, mostly dominated by the rhodophyte Palisada perforata [43]. Our results indicate that these reef tops covered with zoanthids and macroalgae are likely sources of zooplankton, and not sinks, as in many Indo-Pacific coral reefs. Two likely factors are probably boosting the zooplankton abundance at the Tamandaré reef tops: (1) highly productive benthic micro- and macroalgae used as food sources, and (2) vertical habitat compression on the reef tops during the tidal cycle (see above).
In theory, the observed differences could be due to some particular difference in sampling gear, or to some local aggregation of zooplankton at the studied reef edges. Aggregations in downwelling convergence zones could, in theory, be expected at the offshore side of the reef, as in Genin et al. [38]. However, we worked at the onshore side of the reefs, that receives a constant flow of water washed directly from the reef tops at ebb tide. No convergence zones (e.g. accumulation of foam or detritus at a specific spot at the surface) or aggregations (swarms) were observed at these studied edges. Instead, there was a constant horizontal flow of particles and plankton, coming from the slowly emerging reef top. Also, differences in gear used to moor the nets are most likely not the main factor explaining our data, since both gears used are very similar, use the same nets (mesh size, mouth opening, etc.) and sample the same size distributions (as shown by Santos et al. [31]). This supports the idea that the observed differences are not due to method artifacts. Furthermore, the observed differences can be well explained by the characteristics of these highly productive ecosystems, that are covered mostly by macroalgae [43], and occasionally (during the rainy season) receive important nutrient inputs from adjacent rivers. All this evidence supports the idea that these coastal reefs are sources of zooplankton, that is washed from the slightly sloped reef tops towards the nearshore edge at low tide, not sinks.
Origin and composition of coastal reef zooplankton
Compared to the study on macrozooplankton collected with a 300-micron mesh by Santos et al. [31], the present study showed a surprisingly low abundance of meroplankton (i.e., brachyuran crab zoeae). Santos et al. [31] demonstrated that these reefs are the sites of production of large-sized larvae of decapod crustaceans and fish. In the present study, copepods were dominant, and even more surprising, copepods that are not typical for oligotrophic waters, nor typical for tropical coral reefs, but species that are typical for coastal-estuarine waters, such as Parvocalanus crassirostris, although there was no measurable estuarine influence (high salinities and Secchi depths). The predominance of holoplankton indicates that there must be a large abundance of food in the water column. Holoplankton generally feeds in the water column, while early-stage meroplankton contains mostly energy and matter derived from adult benthic populations. These reefs are sites of high density and productivity of organic matter, mainly due to primary producers, such as pelagic and benthic microalgae, detritus from macroalgae and mucus [51,52,53], produced by abundant zoanthids [43]. Zoanthids are also important primary producers, due to their symbiotic zooxanthellae [54].
In spite of strong primary production with zooxanthellae, heterotrophic nutrition in zoanthids does occur [55], where a flat mucous layer that covers the whole organism can be used to trap and absorb sinking particles, such as detritus, invertebrate eggs, and diatoms [56]. This flat mucous layer on the reef surface represents a very different feeding strategy, as compared to most common scleractinian corals, which usually possess a myriad of tentacles that effectively capture zooplankton from the water column. Also, additionally to exporting plankton, the highly productive reefs off Tamandaré have been shown to produce very high densities of several types of biogenic particles [57], that may serve as food for various plankton organisms.
The high contribution of neritic/estuarine and some estuarine species to the zooplankton community at the Tamandaré reefs may indicate that the estuaries formed by the rivers that flow into Tamandaré bay and nearby coastal areas may have an important influence on these coastal reefs, even during the dry season, the time of sampling, when salinities were high and no freshwater outflow to the bay was detectable. One possible explanation is that nutrients (in the form of suspended organic matter) from these estuaries are deposited in surrounding coastal sediments during strong rainfall events, and are then slowly released to the water column in the following dry months.
Among copepods, there are several typical tropical coastal-estuarine species that are commonly found in high densities in estuaries, coastal lagoons and in regions with estuarine influence along the Brazilian coast [23, 28, 58,59,60]: Parvocalanus crassirostris, Dioithona oculata, Oithona hebes, Oithona nana, Pseudodiaptomus acutus, Euterpina acutifrons, Temora turbinata, Oithona oswaldocruzi, and Acatia lilljerborgi. These species also showed greater abundance near the coast, when compared to more distant areas, such as the Abrolhos coral reefs (located 60 km offshore), where they were not found or found only in very low numbers [29, 61, 62].
The high abundance of neritic/estuarine species collected at reef edges may be related to the retention behavior of these species [63,64,65]. In most tidal estuaries, zooplankton exhibits vertical retention strategies according to the tidal cycle, where estuarine plankters migrate towards the bottom when low-salinity waters are flushed toward the sea at ebbing tides. Outflowing freshwater remains closer to the surface. The zooplankton retention near the bottom prevents these organisms from being carried to the sea [63,64,65].
In the present study, the fact that the estuarine-coastal zooplankton was more abundant close to reefs (organisms sampled at reef edge) compared to the open water channels, may also be explained by such retention mechanisms. Samples obtained at reef edges showed a relevant contribution of neritic/estuarine species. This behavior is probably a strategy to avoid a passive drift to unfavorable offshore waters, also to remain in layers with high food concentrations and to increase the likelihood of finding partners [38, 66].
Among the reef-associated organisms are copepod swarms, which were abundantly represented by D. oculata, which is found inhabiting mangrove estuaries, reefs [1, 18, 67] and macroalgal beds [68]. The formation of swarms in this species has the characteristic of being close to structures in the background during the day and dispersion at night [1, 17]. D. oculata can remain in formation at the same site, even in persistent tidal currents, however at night, without swarm formation, copepods are unable to maintain their positions [69] and can be taken by the ebb tide currents. However, as observed in this study, only a significantly smaller portion (3 times less) of this species was transported through the channels out of the reef environment (as seen in the very low abundance at the channels), showing a retention behavior close to the reef substrate.
Another very important reef-associated group were demersal organisms, that can be included into the “reef origin” category, since they emerge in vast amounts from the Tamandaré reef tops at nocturnal high tides [30]. Alldredge and King [70] reported that demersal organisms migrate vertically at short distances. They observed that 80% of the total demersal fauna, especially those of smaller size (< 2 mm), remained 30 cm above the bottom, which is probably due to another type of selective pressure more important than predation, such as water column feeding, reproduction and dispersal [70]. In relation to dispersion, migrating short distances prevents demersals from being taken to the open sea during low tide, where food is scarce and there is no shelter.
Zooplankton exhibits a distinct behavior according to its environment and classification by origin in the reef environment cannot always be easily distinguished, especially for species that inhabit both neritic and estuarine environments. Further studies on the effective contribution of organisms from estuaries to shallow coastal reefs are needed to understand how this influence occurs.
Carbon mass by groups
The highest percentage, in units of carbon mass, in Tamandaré reefs was composed of groups of neritic and estuarine (neritic/estuarine) origin, constituting an important carbon source for upper trophic levels.
The carbon mass of zooplankton at coral reefs is generally much higher at night [12]. This is due to the behavior of demersal organisms that are vertically migrating after dark, pelagic zooplankton entering reefs from the open sea, spawning of some groups such as corals and cessation of predation by visual planktivores such as fish [4,5,6,7,8,9,10,11,12,13,14,15]. However, on the shallow reefs of Tamandaré, the contribution of demersal organisms (i.e., Amphipoda and Cumacea) and the zooplankton of neritic environment was very low.
Total biomass values found in this study were much higher than in studies with pump samplers (mesh 40 μm) near the reefs at night in the Caribbean Sea during summer (3.4 mg C m−3) and for reefs at South Florida (11.8 mg C m−3) [11, 21]. These highly oligotrophic sites, unlike the Tamandaré reefs, have no estuarine influence.
Holoplanktonic organisms were dominant at the reefs of Tamandaré, highlighted by the great abundance of planktonic copepods, which is an important community in many coral reefs [9, 11, 21]. However, they contributed with only 52% of the total carbon mass in Tamandaré reefs, when compared to a Caribbean reef where 68% of the total carbon mass were copepods [11]. This was because the copepods that were dominant at Tamandaré, such as P. crassirostris, D. oculata and O. hebes, have very small body sizes (500 to 600 μm) when compared to species commonly found in other reefs. These animals of larger size contribute with higher carbon mass [9, 21]. Small-sized organisms (100–200 μm) did not show differences in biomass between day and night at Red Sea reefs [12].
The high values of carbon mass found at reef edges compared to channels were also explained to the great participation of groups such as Foraminifera, which are generally caught in resuspension [12] caused by tidal currents that wash the reefs. Another factor was a possible “reproductive peak” of copepods during the study period, leading to a high production rate of copepod eggs and nauplii. Although these nauplii were abundant at the sampling sites, they contributed very little to the biomass [11, 71].