Ivan Nagelkerken

Recent Region-wide Declines in Caribbean Reef Fish Abundance

Profound ecological changes are occurring on coral reefs throughout the tropics, with marked coral cover losses and concomitant algal increases, particularly in the Caribbean region. Historical declines in the abundance of large Caribbean reef fishes likely reflect centuries of overexploitation. However, effects of drastic recent degradation of reef habitats on reef fish assemblages have yet to be established. By using meta-analysis, we analyzed time series of reef fish density obtained from 48 studies that include 318 reefs across the Caribbean and span the time period 1955-2007. Our analyses show that overall reef fish density has been declining significantly for more than a decade, at rates that are consistent across all subregions of the Caribbean basin (2.7% to 6.0% loss per year) and in three of six trophic groups. Changes in fish density over the past half-century are modest relative to concurrent changes in benthic cover on Caribbean reefs. However, the recent significant decline in overall fish abundance and its consistency across several trophic groups and among both fished and nonfished species indicate that Caribbean fishes have begun to respond negatively to habitat degradation.

Coral Larvae Move toward Reef Sounds

Free-swimming larvae of tropical corals go through a critical life-phase when they return from the open ocean to select a suitable settlement substrate. During the planktonic phase of their life cycle, the behaviours of small coral larvae (<1 mm) that influence settlement success are difficult to observe in situ and are therefore largely unknown. Here, we show that coral larvae respond to acoustic cues that may facilitate detection of habitat from large distances and from upcurrent of preferred settlement locations. Using in situ choice chambers, we found that settling coral larvae were attracted to reef sounds, produced mainly by fish and crustaceans, which we broadcast underwater using loudspeakers. Our discovery that coral larvae can detect and respond to sound is the first description of an auditory response in the invertebrate phylum Cnidaria, which includes jellyfish, anemones, and hydroids as well as corals. If, like settlement-stage reef fish and crustaceans, coral larvae use reef noise as a cue for orientation, the alleviation of noise pollution in the marine environment may gain further urgency.

True Value of Estuarine and Coastal Nurseries for Fish: Incorporating Complexity and Dynamics

Coastal ecosystems, such as estuaries, salt marshes, mangroves and seagrass meadows, comprise some of the world’s most productive and ecologically significant ecosystems. Currently, the predominant factor considered in valuing coastal wetlands as fish habitats is the contribution they make to offshore, adult fish stocks via ontogenetic migrations. However, the true value of coastal nurseries for fish is much more extensive, involving several additional, fundamentally important ecosystem processes. Overlooking these broader aspects when identifying and valuing habitats risks suboptimal conservation outcomes, especially given the intense competing human pressures on coastlines and the likelihood that protection will have to be focussed on specific locations rather than across broad sweeps of individual habitat types. We describe 10 key components of nursery habitat value grouped into three types: (1) connectivity and population dynamics (includes connectivity, ontogenetic migration and seascape migration), (2) ecological and ecophysiological factors (includes ecotone effects, ecophysiological factors, food/predation trade-offs and food webs) and (3) resource dynamics (includes resource availability, ontogenetic diet shifts and allochthonous inputs). By accounting for ecosystem complexities and spatial and temporal variation, these additional components offer a more comprehensive account of habitat value. We explicitly identify research needs and methods to support a broader assessment of nursery habitat value. We also explain how, by better synthesising results from existing research, some of the seemingly complex aspects of this broader view can be addressed efficiently.

Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations

Abstract The spatial size distribution of grunts and snappers have previously indicated the separation of juveniles in nursery habitats from the adults on the coral reef. This implies life cycle migrations from nursery habitats (such as seagrass beds and mangroves) to the coral reef. If diet shifts are related to such migrations, then the diets of these fish must change before or around the fish size at which such migrations take place. A wide size range of juveniles of two grunt species ( Haemulon sciurus and Haemulon flavolineatum ) and of two snapper species ( Lutjanus apodus and Ocyurus chrysurus ) were caught in seagrass beds and mangroves, and their gut contents identified and quantified. Regression analysis between fish size and dietary importance of small crustaceans showed a negative relationship in all four species. Positive relations were found for H. sciurus , L. apodus and O. chrysurus between fish length and the dietary importance of decapods, and for L. apodus and O. chrysurus between fish length and prey fish importance. Critical changes in the fish diets with fish size were examined by application of a Canonical Correspondence Analysis (CCA). The CCA yielded three clusters of size-classes of fishes with similar diets, and application of a Mantel test showed that each of these clusters had significantly different diets, and that each cluster diet was significantly specialised. The size at which a fish species ‘switched’ from one cluster to another was compared with size-at-maturity data and with the typical size at which these species migrate from the nursery habitats to the coral reef. H. sciurus and H. flavolineatum may be prompted to migrate from the nursery habitats to coral reef habitats because of dietary changes, or because of the development of the gonads. For L. apodus and O. chrysurus , a dietary changeover forms a more likely explanation for nursery-to-reef migrations than does sexual maturation because these species reach maturity at sizes much larger than the maximum size of individuals found in nursery habitats. Although other factors may theoretically initiate or promote the migration patterns, the results of this study indicate that ontogenetic dietary changes may crucially influence the nursery-to-coral reef migrations of these reef fish species.

Evaluation of Nursery function of Mangroves and Seagrass beds for Tropical Decapods and Reef fishes: Patterns and Underlying Mechanisms

Shallow-water tropical coastal habitats, such as mangroves and seagrass beds, have long been associated with high primary and secondary productivity. The ubiquitous presence of juvenile fish and decapods in these systems has led to the hypothesis that they act as nurseries. Earlier studies mainly focused on the faunal community structure of these systems, leaving us with little detailed insight into their potential role as nurseries. Habitats are considered nurseries if their contribution, in terms of production, to the adult population is greater than the average production of all juvenile habitats, measured by the factors density, growth, survival, and/or movement. High food abundance and low predation risk form the most likely factors that contribute to the attractiveness of tropical nursery habitats. Here, the current state of knowledge on nursery function of shallow-water coastal habitats, particularly mangroves and seagrass beds, is reviewed for each of the above-mentioned factors. Most data show that mangroves and/or seagrass beds have high densities of various fish species and some of their food items, and a lower predation risk for fish and decapods due to factors such as low predator abundance, high water turbidity, and complex habitat structure. In contrast, growth rates of fish appear higher on coral reefs. There is increasing evidence that at least part of the fish or decapod population in these putative nurseries eventually moves away to offshore habitats. The current review shows that mangrove and/or seagrass habitats may act as nurseries through higher juvenile densities and survival rates than offshore habitats, but that trade-offs may exist to the detriment of growth rate. With the lack of detailed movement studies, the exact degree to which mangroves and seagrass beds sustain offshore fish and decapod populations remains largely unclear.

Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses

Biological communities are shaped by complex interactions between organisms and their environment as well as interactions with other species. Humans are rapidly changing the marine environment through increasing greenhouse gas emissions, resulting in ocean warming and acidification. The first response by animals to environmental change is predominantly through modification of their behaviour, which in turn affects species interactions and ecological processes. Yet, many climate change studies ignore animal behaviour. Furthermore, our current knowledge of how global change alters animal behaviour is mostly restricted to single species, life phases and stressors, leading to an incomplete view of how coinciding climate stressors can affect the ecological interactions that structure biological communities. Here, we first review studies on the effects of warming and acidification on the behaviour of marine animals. We demonstrate how pervasive the effects of global change are on a wide range of critical behaviours that determine the persistence of species and their success in ecological communities. We then evaluate several approaches to studying the ecological effects of warming and acidification, and identify knowledge gaps that need to be filled, to better understand how global change will affect marine populations and communities through altered animal behaviours. Our review provides a synthesis of the far-reaching consequences that behavioural changes could have for marine ecosystems in a rapidly changing environment. Without considering the pervasive effects of climate change on animal behaviour we will limit our ability to forecast the impacts of ocean change and provide insights that can aid management strategies.

Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions

Significance People are not only concerned about climate change and its effects on plant and animal diversity but also about how humans are fundamentally changing the globe’s largest ecosystem that sustains economic revenue and food for many countries. We show that many species communities and ocean habitats will change from their current states. Ocean acidification and warming increase the potential for an overall simplification of ecosystem structure and function with reduced energy flow among trophic levels and little scope for species to acclimate. The future simplification of our oceans has profound consequences for our current way of life, particularly for coastal populations and those that rely on oceans for food and trade. Rising anthropogenic CO2 emissions are anticipated to drive change to ocean ecosystems, but a conceptualization of biological change derived from quantitative analyses is lacking. Derived from multiple ecosystems and latitudes, our metaanalysis of 632 published experiments quantified the direction and magnitude of ecological change resulting from ocean acidification and warming to conceptualize broadly based change. Primary production by temperate noncalcifying plankton increases with elevated temperature and CO2, whereas tropical plankton decreases productivity because of acidification. Temperature increases consumption by and metabolic rates of herbivores, but this response does not translate into greater secondary production, which instead decreases with acidification in calcifying and noncalcifying species. This effect creates a mismatch with carnivores whose metabolic and foraging costs increase with temperature. Species diversity and abundances of tropical as well as temperate species decline with acidification, with shifts favoring novel community compositions dominated by noncalcifiers and microorganisms. Both warming and acidification instigate reduced calcification in tropical and temperate reef-building species. Acidification leads to a decline in dimethylsulfide production by ocean plankton, which as a climate gas, contributes to cloud formation and maintenance of the Earth’s heat budget. Analysis of responses in short- and long-term experiments and of studies at natural CO2 vents reveals little evidence of acclimation to acidification or temperature changes, except for microbes. This conceptualization of change across whole communities and their trophic linkages forecast a reduction in diversity and abundances of various key species that underpin current functioning of marine ecosystems.

Yellow band and dark spot syndromes in Caribbean corals: distribution, rate of spread, cytology, and effects on abundance and division rate of zooxanthellae

Yellow band and dark spot syndromes have been frequently observed to affect coral species throughout the Caribbean within the last 10 years. These syndromes significantly impair at least three important reef-building species. Yellow band (also known as yellow blotch) appears as rings or blotches on Montastrea annularis throughout the Caribbean. The coral tissue necrosis occurs at a rate of approximately 0.6 cm/month. Transect measurements at various locations indicated that as many as 90% of M. annularis were affected by yellow band during 1997–98. Tissue samples reveal a 41–96.9% decrease in zooxanthellae/sample compared to healthy specimens, depending on distance from healthy tissue. Mitotic indices (MI) of zooxanthellae (symbiotic algae appearing as doublets) for M. annularis are 2.5%. MI in yellow band samples directly bordering healthy tissue are less than 0.9%, and zooxanthellae directly within the band bordering exposed skeleton had a mitotic index of 0.0%. This indicates impairment of zooxanthellae cell division in yellow band specimens. Zooxanthellae are not expelled and appear vacuolated and devoid of organelles. Dark spot, characterized by tissue necrosis as well as a depression of the colony surface, affects Stephanocoenia michelinii and Siderastrea siderea throughout the Caribbean. Transects showed that as many as 56% of S. michelinii and S. siderea showed signs of dark spot during 1997–98. Affected tissues of S. siderea died at a rate of 4.0 cm/month. In dark spot samples from S. siderea, the total number of zooxanthellae was 56% of that in healthy tissue; dark spot-affected specimens of S. michelinii showed a 14% decrease in the number of zooxanthellae compared to healthy tissue samples. Mitotic indices of zooxanthellae from healthy specimens of S. sidereawere 1.20% compared to 0.40% in dark spot samples. Mitotic indices of healthy S. michelinii were 1.54% compared to 0.23% in dark spot samples, also indicating a decrease in algal cell division. Zooxanthellae from dark spot tissue are swollen and darker in pigment. Due to the changes that are evident in the symbiotic algae, we suggest that both syndromes act primarily on the zooxanthellae symbiont, and secondarily on the cnidarian host.

Mechanisms and ecological role of carbon transfer within coastal seascapes

Worldwide, coastal systems provide some of the most productive habitats, which potentially influence a range of marine and terrestrial ecosystems through the transfer of nutrients and energy. Several reviews have examined aspects of connectivity within coastal seascapes, but the scope of those reviews has been limited to single systems or single vectors. We use the transfer of carbon to examine the processes of connectivity through multiple vectors in multiple ecosystems using four coastal seascapes as case studies. We discuss and compare the main vectors of carbon connecting different ecosystems, and then the natural and human‐induced factors that influence the magnitude of effect for those vectors on recipient systems. Vectors of carbon transfer can be grouped into two main categories: detrital particulate organic carbon (POC) and its associated dissolved organic and inorganic carbon (DOC/DIC) that are transported passively; and mobile consumers that transport carbon actively. High proportions of net primary production can be exported over meters to hundreds of kilometers from seagrass beds, algal reefs and mangroves as POC, with its export dependent on wind‐generated currents in the first two of these systems and tidal currents for the last. By contrast, saltmarshes export large quantities of DOC through tidal movement, while land run‐off plays a critical role in the transport of terrestrial POC and DOC into temperate fjords. Nekton actively transfers carbon across ecosystem boundaries through foraging movements, ontogenetic migrations, or ‘trophic relays’, into and out of seagrass beds, mangroves or saltmarshes. The magnitude of these vectors is influenced by: the hydrodynamics and geomorphology of the region; the characteristics of the carbon vector, such as their particle size and buoyancy; and for nekton, the extent and frequency of migrations between ecosystems. Through a risk‐assessment process, we have identified the most significant human disturbances that affect the integrity of connectivity among ecosystems. Loss of habitat, net primary production (NPP) and overfishing pose the greatest risks to carbon transfer in temperate saltmarsh and tropical estuaries, particularly through their effects on nekton abundance and movement. In comparison, habitat/NPP loss and climate change are likely to be the major risks to carbon transfer in temperate fjords and temperate open coasts through alteration in the amount of POC and/or DOC/DIC being transported. While we have highlighted the importance of these vectors in coastal seascapes, there is limited quantitative data on the effects of these vectors on recipient systems. It is only through quantifying those subsidies that we can effectively incorporate complex interactions into the management of the marine environment and its resources.

A test of the senses: Fish select novel habitats by responding to multiple cues

Habitat-specific cues play an important role in orientation for animals that move through a mosaic of habitats. Environmental cues can be imprinted upon during early life stages to guide later return to adult habitats, yet many species must orient toward suitable habitats without previous experience of the habitat. It is hypothesized that multiple sensory cues may enable animals to differentiate between habitats in a sequential order relevant to the spatial scales over which the different types of information are conveyed, but previous research, especially for marine organisms, has mainly focused on the use of single cues in isolation. In this study, we investigated novel habitat selection through the use of three different sensory modalities (hearing, vision, and olfaction). Our model species, the French grunt, Haemulon flavolineatum, is a mangrove/seagrass-associated reef fish species that makes several habitat transitions during early life. Using several in situ and ex situ experiments, we tested the response of fish toward auditory, olfactory, and visual cues from four different habitats (seagrass beds, mangroves, rubble, and coral reef). We identified receptivity to multiple sensory cues during the same life phase, and found that different cues induced different reactions toward the same habitat. For example, early-juvenile fish only responded to sound from coral reefs and to chemical cues from mangroves/seagrass beds, while visual cues of conspecifics overruled olfactory cues from mangrove/seagrass water. Mapping these preferences to the ecology of ontogenetic movements, our results suggest sequential cue use would indeed aid successful orientation to novel key habitats in early life.