Coral Reefs DOI 10.1007/s00338-013-1075-4
NOTE
The influence of natural cycles on coral reef fish movement: implications for underwater visual census (UVC) surveys J. P. Bijoux • L. Dagorn • J.-C. Gaertner P. D. Cowley • J. Robinson
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Received: 29 May 2012 / Accepted: 19 August 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract Movement patterns of some coral reef fishes change with natural cycles (e.g., tidal, lunar and seasonal), resulting in short-term shifts in fish assemblages. We reviewed the literature on temporal changes in coral reef fish assemblages derived from underwater visual census (UVC) and found that movement was rarely considered in experimental design and analysis or as cause of change in interpretation of the results. Studies of vagile species, large individuals, species forming transient spawning aggregations and studies of fishes in contiguous habitats are most likely to be affected by such movements. Ignoring predictable patterns of movement associated with such natural
Communicated by Biology Editor Dr. Hugh Sweatman
Electronic supplementary material The online version of this article (doi:10.1007/s00338-013-1075-4) contains supplementary material, which is available to authorized users. J. P. Bijoux (&) L. Dagorn UMR 212 EME, Institut de Recherche pour le De´veloppement, Victoria, Mahe´, Seychelles e-mail:
[email protected] J.-C. Gaertner UMR 241 EIO, Institut de Recherche pour le De´veloppement, Papeete, Polyne´sie franc¸aise P. D. Cowley South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown, South Africa J. Robinson Seychelles Fishing Authority, P.O. Box 449, Victoria, Seychelles J. Robinson ARC Centre of Excellence for Coral Reef Studies, Townsville, Australia
cycles in survey design and analysis increases ‘‘unexplained’’ variation, making it more difficult to detect longer-term changes in fish assemblages and reducing the effectiveness of UVC as a monitoring tool. Keywords Fish movement Temporal change Coral reef fishes Short-term natural cycles Underwater visual census
Introduction Change in coral reef fish assemblages over time is often assessed on the basis of fish abundance, biomass and diversity (McClanahan et al. 2007a; Russ and Alcala 2010). Many studies concern changes in these variables on timescales of years to decades resulting from human or natural impacts to reefs, but fish assemblages also vary naturally on short timescales of minutes to seasons (Thompson and Mapstone 2002; McClanahan et al. 2007b). Variation caused by these short-term, intra-annual cycles may influence the ability to detect temporal changes in fish assemblages occurring over longer periods (e.g., years or decades). Consequently, it is necessary to distinguish variation in fish assemblages due to movement in response to intra-annual natural cycles, and other sampling errors (e.g., inaccurate estimation of survey area), from those due to changes in recruitment, mortality and growth that result from the impacts being investigated (Thompson and Mapstone 2002). Fish movement is an important source of variation in coral reef fish assemblages (e.g., McClanahan et al. 2007b). Changes in fish assemblages are often associated with short-term natural cycles (tidal, lunar, seasonal) that provide strong and predictable cues influencing fish behaviour
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(Craig 1996; Meyer et al. 2007; Claydon et al. 2012). Variation in fish assemblages can be extreme, particularly when changes caused by natural cycles are correlated with time, for example, when fish aggregate to spawn on a particular lunar phase within a specific season (Robinson et al. 2008; Bijoux et al. 2013). In spite of its importance in structuring assemblages, species behaviour continues to be neglected in ecological research and conservation practice (Shumway 1999; Angeloni et al. 2008). In this note we discuss how variation in reef fish behaviour relates to short-term natural cycles and examine the extent to which change in assemblages has been attributed to fish movement caused by those cycles in the literature. The results of the literature review are used to identify which components of reef assemblages (e.g., functional groups) and which types of studies are likely to be affected by variation in fish movement. To conclude, we provide recommendations for integrating variation in fish movement in underwater visual census (UVC) design and data analysis.
Materials and methods Studies used in the literature review were identified based on keyword search in the Web of Science database (last accessed 30 October 2011) supplemented by searches using Google Scholar. The keywords reef fish, temporal change and time series were used singly or in combination. The searches were refined using keywords relating to some of the main drivers of temporal change addressed in ecological studies of coral reef fish communities, such as MPAs, fishing, pollution, disturbance, hurricane, cyclone, movement, mobility, behaviour, season and manipulation. We only considered studies based on UVC surveys of adult fishes in coral reef habitats that were published in the last 30 years (1981–2011). We included observational studies as well as studies in which one or more components of the fish assemblage or habitat had been manipulated. All study durations, geographical areas, sampling frequencies, species and UVC methods were considered, provided that the same sites were sampled on at least two occasions. This included studies in which data were collected by the same observer and those where observers changed over time, as in many long-term monitoring programmes. We included studies that surveyed whole assemblages, parts of assemblages or single populations. Methodological papers were excluded. The final list consisted of 88 published studies. These studies were categorised according to the main proximate cause of the assemblage change that they identified and were used to assess how frequently fish movement associated with short-term natural cycles has been considered as an explanation for temporal change in coral reef fish assemblages. The causes of change were as
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follows: (1) top-down effects, (2) bottom-up effects, (3) mixed top-down and bottom-up effects and (4) effects of fish movement. A fifth category included studies for which the causes of change were not clearly defined. Top-down causes of change were those resulting from direct human intervention such as fishing or protection through no-take zones. Bottom-up causes of change were those affecting reef fish assemblages through physical change to habitat even if the ultimate cause was anthropogenic, e.g., reef degradation due to climate change. The mixed category combined studies where both top-down and bottom-up causes were identified. Proximate causes relating to movement were considered when changes in fish assemblages were explicitly due to temporary movement of fish into or out of the survey area.
Fish movement and temporal change in assemblages Most temporal changes in coral reef fish assemblages were attributed to bottom-up (37 studies) and top-down causes (36 studies) (Electronic Supplemental Material, ESM Table S1). Three studies attributed observed temporal changes to a mixture of top-down and bottom-up causes, and the proximate cause of change was not clearly defined in six studies. Only six studies attributed the observed changes, either wholly or partially, to the effects of fish movement, and all these were designed a priori to investigate the effects of short-term natural cycles on assemblages. These studies revealed that tidal, lunar and seasonal variations in fish movement are responsible for large changes to coral reef fish assemblages. It is surprising that so few of the remaining studies considered the variation caused by natural cycles on fish movement in the experimental design. For instance, only three studies provided details of the lunar timing while six papers gave the diel timing of surveys. Remarkably, 30 papers did not even state the month of the surveys. It is possible that many of the studies did account for temporal variation in fish movement in their survey design but did not report this. Examples of studies that did incorporate sources of temporal variation in experimental design include surveys standardised for season, based on the known periods of high movement of certain species (Brokovich et al. 2006), and surveys sampling the same months (Russ and Alcala 2010) or stage of the tide (McClanahan and Kaunda-Arara 1996).
Relative importance of different short-term natural cycles In order to consider the effects of fish movement in the design of surveys, reef fish ecologists need to know how much of the
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highlighted the relative importance of lunar and seasonal cycles on fish assemblages (Fig. 1b, c; e.g., Letourneur 1996). However, McClanahan et al. (2007b) note that nearinstant variation in fish assemblages (i.e., that occurring on a scale of minutes) is sufficiently large (15–25 %) that detecting the influence of intra-annual cycles may be problematic. The expanding use of acoustic telemetry in long-term studies of fish behaviour may help resolve the relative importance of different sources of variation in fish movement.
Components of reef fish assemblages and types of study that are likely to be affected by fish movement Fish movement is greater in larger species and in larger individuals (Kramer and Chapman 1999; Jones 2005). Letourneur (1996) noted that more vagile fish genera such as Mulloides, Ctenochaetus, Siganus and Scarus showed higher variation in density associated with the lunar phase than less vagile genera such as Dascyllus and Zebrasoma. If larger species and larger individuals are more likely to show cyclical patterns of movement, then studies of topdown processes may be particularly prone to movement effects since these processes selectively affect larger fishes. Temporal changes caused by top-down processes tended to concern larger species than those associated with bottomup processes (Fig. 2). Consequently, studies focusing on human interventions such as fishing and protected area effects will need to consider how to account for predictable patterns of movement by the larger species or individuals. Functional ecology of species also influences the degree of
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variation in assemblages is associated with different shortterm cycles. An exhaustive review of the subject is beyond the scope of this note, but a few studies provided some insights. None of the six studies that addressed this issue explicitly (Lewis 1986; Galzin 1987; Letourneur 1996; Ault and Johnson 1998; Thompson and Mapstone 2002; McClanahan et al. 2007b) compared the effect of variation in fish abundance resulting from all short-term cycles considered here (i.e., tidal, lunar, seasonal) on the ability to detect interannual trends. The study of Thompson and Mapstone (2002) came closest by comparing diurnal, daily and monthly effects on variation in the abundance of several fish species and families, but daily sampling was not aligned to different lunar phases. Nevertheless, they found that variation in fish abundance between days caused by movement accounted for a large proportion of the overall intra-annual variation (mean = 69.6 %). In species that are known to feed and migrate with the tide, high daily variation in abundance may result from sampling different times of the day (Thompson and Mapstone 2002). However, nested within diurnal and daily variation, which may relate to tides depending on species, fish assemblages also vary on a scale of minutes (McClanahan et al. 2007b). While variation in fish assemblages may be high on short temporal scales (Thompson and Mapstone 2002; McClanahan et al. 2007b), it is compounded with variation occurring on longer timescales such as lunar phase and season. Thompson and Mapstone (2002) found that daily variation in abundance was highest for the Lutjanidae, Serranidae and Siganidae. Many species from these families are highly mobile foragers (Meyer et al. 2007; Fox and Bellwood 2011), which would account for diurnal and daily variation, but they may also make larger-scale spawning migrations at particular lunar phases and seasons (Sadovy de Mitcheson et al. 2008). Distinguishing the variation in abundance due to reproductive and non-reproductive movement requires daily sampling nested within lunar and seasonal (spawning versus non-spawning seasons) periods. The study of Letourneur (1996) came close to such a design and attributed high levels of lunar variation to spawning behaviour, though this was not quantified. Galzin (1987) found that 30.7 % of variance related to the lunar cycle and 37.5 % concerned semi-lunar periodicity in fish abundance, though lunar sampling was not nested within season. Knowing how much variation in fish abundance is associated with different short-term cycles would enable sampling designs to be tailored for specific species, families or other groups depending on their behaviour. Variance is accumulated across temporal scales (Thompson and Mapstone 2002), but patterns of movement on different timescales may have different relative importance. Some studies have found that longer-term intra-annual cycles contribute less variance than daily cycles (Fig. 1a; e.g., Thompson and Mapstone 2002), and others have
20 0 Tidal cycle
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Seasonal cycle
Fig. 1 Conceptual figure representing three patterns of variance in coral reef fish abundance associated with the tidal, lunar and seasonal cycles. Variation due to the three cycles is additive, and the variation associated with each cycle is equivalent to the area under each step. Traces represent situations where the (a) tidal, (b) lunar and (c) seasonal cycles contribute the greatest variation. The height and shape of the steps are examples and would vary among species and populations depending on the relative influence of the three cycles on their movement
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Bottom-up causes
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Fig. 2 Percentage of fish species in 10-cm-size categories that changed significantly in the studies for which top-down and bottomup proximate causes were identified as being responsible for the observed temporal changes in fish assemblages. Data are extracted from studies listed in ESM Table S2. Only species showing significant temporal change and those specifically identified as driving the observed temporal changes are included. Maximum species fork lengths are derived from FishBase (www.fishbase.org). Due to the predominance of papers that identified top-down and bottom-up effects as the cause of temporal changes in coral reef fish assemblages, the other categories could not be thoroughly evaluated in this analysis
fish movement (Nash et al. 2013), so functional groups containing vagile species (e.g., roving piscivores and herbivores) are more likely to be affected by variation in movement of species than functional groups containing sedentary species with small home ranges (e.g., small ambush predators). This is supported by the six studies in our review that identified movement as a primary explanation for observed temporal change in fish assemblages. For example, McClanahan et al. (2007b) showed that the abundance of more vagile scarids and acanthurids is associated with higher levels of near-instant variation than that for sedentary pomacentrids. Many reef fishes migrate to specific sites to spawn at particular lunar phases in particular seasons (Robinson et al. 2008; Bijoux et al. 2013). Spawning migrations can be extensive and will cause abundance to increase at spawning sites (Rhodes and Sadovy 2002; Robinson et al. 2008; Bijoux et al. 2013) while decreasing at home sites. Some studies in our review suggested that movement related to reproduction could be a cause for temporal change in abundance or density (Galzin 1987; Letourneur 1996). Hence, failure to standardise for lunar phase or season may confound results if fish are departing, migrating through or arriving in survey areas in large numbers to spawn. Such effects will be more noticeable in species that form transient rather than resident spawning aggregations, as the former tend to involve greater migration distances and endure for longer periods of the month. By definition,
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resident spawning aggregations draw individuals to spawning sites located within or nearby their adult home range (Domeier 2012) and so occur over spatial scales similar to UVC counts (Claydon et al. 2012). Movement associated with transient spawning aggregation formation is more difficult to account for in spatial survey design and requires standardisation for lunar phase and season. None of the studies considered the effect of habitat on fish movement and abundance. Habitat characteristics can influence movement of coral reef fishes and may play an important role in regulating the extent of movement associated with natural cycles on a variety of temporal scale. Scarids and acanthurids migrate between the back reef and reef slope at sunrise and sunset (Lewis 1986). Certain species move onto large inter-tidal habitats during high tide, causing changes in abundance on the reef slope with the tide (e.g., Craig 1996). Some species are reluctant to leave coral substratum and cross large expanses of dissimilar habitat such as sand (Chapman and Kramer 2000). Consequently, the extent and configuration of preferred habitat can regulate movement and dictate home ranges. For example, several coral reef species have more elongated home ranges on fringing reefs than in patch reef environments (Zeller 1997; Eristhee and Oxenford 2001). This suggests that coral reef fishes inhabiting contiguous habitats, such as fringing reefs, are more likely to be affected by fish movement resulting from short-term natural cycles than those in discontinuous habitats, such as patch reefs.
Integrating natural cycles into survey design and data analysis As movement associated with natural cycles is a source of variation in coral reef fish assemblages, it is important to consider the practical implications of this for the collection and analysis of UVC data. Several manuals for UVC surveys are available (e.g., English et al. 1997; Samoilys 1997), but these do not emphasise importance of standardising surveys with regard to natural cycles, apart from avoiding crepuscular periods. Our review found that this source of variation was rarely considered, or at least underreported, in the published literature. High-frequency (tidal) and low-frequency (seasonal) cycles may be easier to incorporate into a survey design than medium-termfrequency (lunar) cycles. It is relatively easy to repeat a survey at the required tidal state in the event that a planned survey is missed, and timing surveys to a particular season is straight forward. By contrast, repeating a missed sample for a particular phase of the moon would require waiting approximately 21 days, which is not well suited to the typical length of field trips. If natural cycles cannot be
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incorporated into the survey design, then state of tide, lunar phase and season should be included as potential sources of variation in the analysis. Circular statistics can be used to investigate short-term cyclic periodicity in fish abundance (e.g., Findlay and Allen 2002), and periodic regression has been suggested as a more sensitive and robust technique for examining cyclical patterns over more commonly used categorical ANOVA (deBruyn and Meeuwig 2001). Harmonic analyses such as Fourier and continuous wavelet transform analysis have also been successfully used to identify periodicity patterns in time-series data (ManjarresMartinez et al. 2010; Alo´s et al. 2011) and could be applied in studies that collect data on temporal scales appropriate to natural cycles (e.g., Galzin 1987; Letourneur 1996). When statistical tests identify variation aligned with natural cycles, the literature on behavioural ecology will be useful in interpreting results. Acoustic telemetry is increasingly used to identify movement relating to habitat usage (Fox and Bellwood 2011) and other behavioural processes, such as reproduction (Bijoux et al. 2013), and could be used to quantify the level of assemblage variation associated with different cycles. For example, monitoring the presence and absence of acoustically tagged fish at foraging sites during different tidal phases or at spawning sites during different lunar phases would, respectively, allow for the quantification of tidal and lunar effects on species abundance. Not all reef fish species are suited to UVC techniques (Jennings and Polunin 1995) and behavioural ecology may ultimately identify the survey constraints for a wide range of reef fish species in relation to their movement and habitat usage. In conclusion, our review found that fish movement associated with diurnal, tidal, lunar and seasonal cycles is rarely considered in studies of temporal change in reef fish assemblages. This defies the considerable evidence that this aspect of behaviour is important to the structure of assemblages, particularly for larger species that forage widely and migrate to spawn. More information is required on movement of species in response to a range of shortterm cycles if this source of variation is to be partitioned from change resulting from processes that affect species survival and growth, such as fishing. Acknowledgments We thank NAJ Graham for providing helpful comments on earlier versions of this manuscript. The manuscript was improved by comments from the Topic Editor and two anonymous reviewers. This publication was made possible through support provided by the IRD–DSF to JPB.
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