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Grouper spawning aggregations: Be careful what you measure and how you measure it: A rebuttal of Golbuu and Friedlander (2011)
Estuarine, Coastal and Shelf Science 123 (2013) 1e6
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Grouper spawning aggregations: Be careful what you measure and how you measure it: A rebuttal of Golbuu and Friedlander (2011) Patrick L. Colin a, *, Yvonne Sadovy de Mitcheson b, Terry J. Donaldson c a
Coral Reef Research Foundation, P.O. Box 1765, Koror, PW 96940, Palau School of Biological Sciences, University of Hong Kong, Puk Fu Lam Road, Hong Kong c University of Guam Marine Laboratory, UOG Station, Mangilao, GU 96923, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 May 2011 Accepted 13 October 2011 Available online 2 November 2011
Golbuu and Friedlander (2011, Estuar. Coast. Shelf Sci. 92:223) used faulty methods, improper interpretation of historical data, and assumptions of little or no validity to conclude that despite protected status spawning aggregations of three groupers in Palau, western Caroline Islands declined between 1995e96 and 2005e06. Alternate survey methods indicated no drastic declines in these aggregations over the same period. Golbuu and Friedlander (2011) failed to document the overall distribution of fishes in their aggregations, used poorly-located inadequate transects to sample the overall aggregation area, and did not identify and sample peak aggregations days. The use of visual length estimates as the basis for biomass values may introduce errors. Comparison of aggregation persistence between reference (“fished out”) and protected sites is not possible because equivalent protected and exploited sites are not available. Different species at multi-species spawning aggregation sites commonly occupy somewhat discrete locations, with the densest concentrations (core areas) of one often being separated from those for another. There is usually a single peak day each month of a lunar-based aggregation, but it requires multiple days data collection to determine that peak. The shortcomings identified provide important lessons for the study of fish spawning aggregations and signal caution about the incomplete documentation of sampling methodology. Overly simplistic aggregation sampling methodologies may be superficially credible, but are not reflective of a complicated reality. Monitoring needs to produce a definitive repeatable baseline against which data can be gathered authoritatively in the future. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: spawning aggregation grouper Palau survey methods traditional ecological knowledge conservation
1. Introduction In a recent paper in this journal, Golbuu and Friedlander (2011) presented data regarding the density and distribution/abundance of three species groupers (Pisces: Serranidae) at spawning aggregations in the Republic of Palau in the western Caroline Islands. Based on their data they concluded that, despite protections of various types, populations of these groupers underwent declines in numbers of fishes aggregating at two sites in 2005e2006 compared to a decade earlier (1995e1996) based on the unpublished report of Johannes et al. (1999) for the same sites. Unfortunately we must reject the conclusions of Golbuu and Friedlander (2011) as they are based upon faulty methods for monitoring fish spawning aggregations, improper interpretation of historical grouper data, and numerous assumptions of little or no validity. We believe that their
* Corresponding author. E-mail address: [email protected] (P.L. Colin). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.10.011
results, therefore, cannot be used to conclude anything about the status of these aggregations in Palau. The three grouper species (brown-marbled grouper e Epinephelus fuscoguttatus, camouflage grouper e Epinephelus polyphekadion and squaretail coralgrouper e Plectropomus areolatus) are often found aggregating at the same locations and times. These are “transient aggregations” (Domeier and Colin, 1997), meaning that fish engage in movements from home territories and remain at the aggregation site for a period of some days, usually on a lunar and seasonal basis. These spawning aggregations are the only time that these species, which support important fisheries at nonaggregation times, are known to reproduce and have variously received protection in the last two decades. Hence, using scientifically credible methods for the assessment of their status is important for understanding fisheries, and the effectiveness of management interventions. Spawning aggregations of these three species have been known in Palau historically as traditional ecological knowledge (TEK) that had been documented by Johannes et al. (1999) and Johannes (1981). Their unpublished
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report forms the starting point for evaluation of population changes by Golbuu and Friedlander (2011). 2. What are the problems? The monitoring of spawning aggregations for fish abundance and densities is challenging and depends on applying a welldesigned sampling protocol that is representative, clear and replicable. The Society for the Conservation of Reef Fish Aggregations (SCRFA) has made efforts to promote appropriate and repeatable methods for quantifying fish spawning aggregations. Spawning aggregations of groupers are quite variable in time and space within single sites and between multiple sites, thus it is critical to develop a sampling protocol with the appropriate time period, spatial coverage and sampling methodology, especially for multispecies aggregations (Colin et al., 2003; Colin, 2011). In the past few years work has been undertaken by SCRFA with the Palau Conservation Society (PCS) to better quantify grouper spawning aggregations in the Republic of Palau with some success (PCS/ SCRFA, 2010), including at one of the two sites (Ebiil) reported in Golbuu and Friedlander (2011) study. In addition, two of us (PCL and TJD) have used similar survey techniques at the second aggregation site (Ngerumekaol) from 2003 to 2010, with particularly intensive survey work in 2005 (Colin et al., 2005). The first step in planning any sampling regime for aggregation fish density and abundance, as well as to ensure replicability, is to determine the limits and general distribution of the aggregated fish(es). Within the aggregation area, numbers and density of fish, sex ratios, and size of individuals can change within a single day, between days, among lunar months, and on a seasonal basis. Appropriate and consistent sampling protocols should be used to make meaningful comparisons across time at any aggregation site. Isolated densities of fish(es) within an aggregation cannot be used as a meaningful measure of abundance if they vary across aggregation sites. Typically species have areas of higher density toward the center of the aggregation (core) and lower densities at the edges (Samoilys, 1997; Rhodes and Sadovy, 2002; Nemeth et al., 2007), and this is known for the groupers presently under consideration Therefore, fish numbers are best reported in terms of abundances, ideally based on a series of density measurements encompassing most to all of the aggregation. We question the methods and analysis of Golbuu and Friedlander (2011) to characterize the abundance of three groupers at the two study aggregation sites, then to draw conclusions regarding changes in aggregation numbers and hence the effectiveness (positive or negative) of management relative to the earlier study at the same sites. Additionally we doubt the study in question can be replicated, as the methods, locations and sampling times used are not adequately described. We believe also that the shortcomings of this research provide very important lessons in relation to the study of aggregations in general that cannot be ignored, as well as signal caution about the incomplete documentation of sampling methodology. We base our concerns primarily on an evaluation of the methodology provided by Golbuu and Friedlander (2011) and with support from results from other studies at the research sites involved (Johannes et al., 1999; Colin et al., 2005; Colin and Donaldson, in preparation; PCS/SCRFA, 2010), as well as on the same species elsewhere (Rhodes and Sadovy, 2002; Sadovy, 2005). Concerns arising from the study of Golbuu and Friedlander (2011) fall into seven areas; specifically:: (a) the use of isolated density as a measure of aggregation size and abundance; (b) the lack of specific details on the placement of transects relative to the total aggregation area implying an inability to meaningfully document either density or abundance; (c) the lack of replicability; (d)
the methods used to assess body size to evaluate changes between the present and past studies; (e) the use of a single day each month for sampling; (f) the overall conclusions regarding changes in aggregation status (compared with the Johannes et al., 1999), as well as comparison with “reference” sites; (g) conclusion that there was an unequivocal loss of camouflage grouper from the Ebiil site. 3. Measurement of aggregation size, fish numbers and density within aggregations, placement of transects and concerns about replicability Golbuu and Friedlander (2011) reported on surveys of two grouper aggregation sites in barrier reef channels, Ebiil and Ngerumekaol (also known as “Ulong Channel”), plus two reported former aggregation sites (called “reference areas”), Ngebard and Rebotel, monthly for 18 months. They indicate “surveys were conducted once a month, sometime 2e6 days before the new moon, which coincides with peak in aggregation density of several grouper species in Palau”, but did not identify any specific days before new moon (BNM) when surveys were conducted. We interpret this to mean transect surveys were done only on one day each month during that 2e6 days BNM period. Johannes et al. (1999) reported for each lunar month a peak in the number of fishes to aggregate on a single day sometime within this period, 2e6 days BNM, but the peak day was unpredictable. Golbuu and Friedlander (2011) surveyed five 50 5 m permanent transects (250 m2 each) at an unspecified depth at each site for the numbers of groupers, plus an assortment of other fishes. The locations and relationships of the transects were not provided. Sizes of fishes were estimated visually and estimates of total biomass of each species obtained from these estimated lengths using the lengtheweight relationships appearing in FishBase (fishbase.org). Golbuu and Friedlander (2011) did not elaborate further on how the transect sites were chosen, whether they were in a continuous line or separated from one another nor their relationship to the total area of aggregation of the three species. Three major problems stem from the inability of the five relatively short transects at each site, particularly if they are in a single line, to capture adequately the distribution and density of fishes that vary spatially both within and between species. Moreover, because Golbuu and Friedlander (2011) did not delimit the outer boundaries of the aggregation sites for the three study species, the placement of transects relative to their distributions or core areas is unknown. First, those authors state that placement of their five transects were in the same general locations as in the earlier Johannes et al. (1999) study. However, in Johannes et al. (1999) (one of the co-authors of which was YS) a core area for monitoring was simply delineated to include the largest proportion of the aggregation that it was possible to count on a dive with a single SCUBA tank by one person. This was an unknown proportion of the total aggregation and consisted mainly of Plectropomus areolatus, with Epinephelus polyphekadion less thoroughly covered because these fish were too deep to monitor fully. Second, Johannes et al. (1999) conducted a zigzag survey (not on a particular line) between rebar markers at the Ebiil site rather than a specific transect. Specific transects were also not indicated for Ngerumekaol, just that numbers of fish were monitored both in the channel and in the northern area near the channel mouth. Third, by limiting sampling to (apparently) one day per month for each aggregation it is uncertain whether the day of peak fish abundance (density) was sampled and this prevents valid comparisons between months and years. Although peak densities have been known to occur sometime within the period 2e6 days BNM, it is not consistent which day that is from month to month or between aggregation sites. It should be noted also that density in a small area is not necessarily proportional to total fish numbers.
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Golbuu and Friedlander (2011) sampled an unknown proportion of their study aggregations on a day of unknown relationship to peak densities for the month/year of study. This undoubtedly resulted in biased and flawed data that formed the basis for invalid conclusions and overall their surveys are not, given the present information, replicable by others. Short transects relative to the overall aggregation area for the study species are not recommended as a method of monitoring aggregation fishes (Colin et al., 2003), particularly for multi-species aggregations when the overall distribution of fishes is not known. The short transect methods used by Golbuu and Friedlander (2011) were not directly comparable to the earlier Johannes et al. (1999) study in survey pattern, placement or dimension. In general such short transect methods are not suitable for surveying fish spawning aggregations because their numbers, size and placement are critical. The densities of fishes within only a small portion of an aggregation cannot be used reliably for obtaining representative samples as a measure of total abundance, as fish density varies across the aggregation and decreases toward the edges of an aggregation. This is particularly true for multi-species aggregation, such as those of concern here, as different species have somewhat different distributions within an overall site. Also the overall area an aggregation occupies decreases with lower total fish numbers. During a large aggregation those areas outside the core of the aggregation would have densities lower than those of fish in the core, but during an aggregation with fewer fish (and a smaller overall area) these same areas might totally lack fish, although densities of fish are still high in the core area. We also believe the use of visual length estimates as the basis for biomass values may introduce substantial errors at multiple levels, but that cannot be determined. The conversion of estimated length of groupers to biomass is further complicated with fish present in spawning aggregations are generally larger individuals with considerable variation in body weight (as much as 2 times) for a given length (for example see Sadovy and Eklund, 1999), hence using estimated length to determine biomass of a group of fishes is dubious, and accuracy of data unknown. More appropriate (but still with inherent errors) would have been the comparison of size frequency histograms at 5 cm intervals for Plectropomus areolatus with those of Johannes et al. (1999), but this was not done. The use of uncertain biomass values rather than fish abundance also fails to describe adequately the characteristics of a spawning aggregation. Even if length and consequently weight data were accurate, a few large, heavy fish might comprise a given aggregation but the actual size of the aggregation would be smaller compared to one with many smaller but reproductively active fish; this distinction has consequences for determining both population size and the overall reproductive potential of the aggregation, especially if sex-specific body sizes (e.g., males larger than females) and sex ratios are skewed.
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site (more on this subject below), yet there are also large areas that have either a single species present, or the others at very low densities (Fig. 1). The outer limits were determined by using GPS surveys (Colin et al., 2005; Colin, 2011) to delineate boundaries beyond which groupers ceased to occur (PCS/SCRFA, 2010). The density of fish within the aggregation increases toward its central area (Fig. 2) and a few short transects placed haphazardly within the overall aggregation area will almost certainly produce a highly biased sampling of fish numbers. In a worst case, a species may be totally missed by poor selection of transects locations, such as that of the original PCS transect (Fig. 2) and presumably the Golbuu and Friedlander (2011) transect locations. In addition to the problem of differing overall distributions for species, the density of a single species within an aggregation differs and decreases from a central (i.e. core) area to zero at the edges of the aggregation (Fig. 2). To measure the highest density within an aggregation on any given day it is necessary to know where that location is, otherwise measuring density on short transects does not provide an estimate of total numbers or biomass within an aggregation. Data from GPS density surveys indicate that the same location is not always the area of highest density on different days. Interestingly, the role of geomorphology in individual species distributions is well illustrated in Fig. 1. At Ebiil (Fig. 1a) the three
3.1. Different grouper species tend to occupy different areas within spawning aggregation sites Different fish species at multi-species spawning aggregation sites commonly occupy somewhat discrete locations, with the densest concentrations (core areas) of one species often being separated from such areas for another. Within a multi-species site, the overall distribution of a species, however, often overlaps into aggregation areas of another species to the point so that the multiple species form a continuous area occupied by one or more species. This is typical for the three grouper species that form spawning aggregations at the two active Palau spawning aggregation sites, especially Ebiil (Colin et al., 2003, 2005; PCS/SCRFA, 2010). There are areas of overlap, particularly at the Ngerumekaol
Fig. 1. Geographic limits of spawning aggregations of three grouper species typical of days of peak aggregation at (a) Ebiil channel, and (b) Ngerumekaol channel, Palau. Areas were surveyed with the GPS density method and limits shown are based on surveys conducted on a single peak day in 2009 for Ebiil (PCS/SCRFA, 2010) and in 2005 for Ngerumekaol (Colin and Donaldson, unpublished data). The location of transects of Golbuu and Friedlander (2011) within these areas are not known, however the scale distance scale shown for both areas is divided into 50 m increments to indicate the relative length of 50 m transects compared to the overall distribution of fishes.
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3.2. The peak day of aggregation varies and it is necessary to survey multiple days to determine peak day
Fig. 2. Example of a GPS density bubble plot for Epinephelus polyphekadion during a peak spawning day at Ebiil Channel, Palau showing the decrease in density away from the central “core” area and outer limits of the aggregation. Empty circles are areas with no fish. The location of the original Palau Conservation Society transect (200 m in length) is shown to indicate how a species would be missed by a poorly placed short transect.
groupers occur along the southern reef slope at the mouth of the channel with the bathymetry indicated. These groupers have been reported to have formed spawning aggregations previously along the north-side slope, but they no longer do so (Johannes et al., 1999). The channel mouth reaches at least 35 m in depth, becoming sandy on the middle flat section, and the groupers occur only along the reef-covered slope and do not go below ca. 30 m. When numbers of individual fishes are high (Fig. 1a), the distributions of the three species overlap somewhat. When fish numbers are lower, the overlap is minimal or does not exist, with the aggregation of each species centered on the core area of its individual distribution. This can be seen in the overall PCS/SCRFA Ebiil data (PCS/SCRFA, 2010, Figs. 5 and 11). At Ngerumekaol, the channel is shallower, with lush reef generally about 9e12 m in depth across the channel mouth, with sides or walls that slope steeply upward to a reef flat only 1e2 m deep. The aggregation area includes both sides of the channel as well as the central bottom area (Fig. 1b). While the three species still have somewhat different distributions that are maintained throughout the aggregation season, there is more overlap in their occurrence compared to Ebiil. The distribution of Epinephelus fuscoguttatus is centered on the channel bottom area about 200e300 m inside the mouth and fish are not common up the channel sides. The highest densities of the other two species are found both on the channel bottom and also up the sides of the channel, however, the population of E. polyphekadion is located closer to the channel mouth, while Plectropomus areolatus extends much further into the channel. If even higher numbers of fishes were present, these relative distributions might change. Johannes et al. (1999) clearly encountered all three species of groupers at the Ebiil site and the data they presented on relative abundance for 1995e1996 (Epinephelus fuscoguttatus e 21e19%, Epinephelus polyphekadion e 43e52%, Plectropomus areolatus e 3528%) indicate all species are common in the aggregations. Johannes et al. (1999) conducted surveys down to 35 m depth and as such would have encountered the deeper E. polyphekadion aggregation missed by Golbuu and Friedlander (2011). Indeed, they reported maximal counts of E. polyphekadion at Ebiil of over 900 fish.
Knowledge of exactly when the numbers of fish within an aggregation for each species peaks before the new moon is imperfect. Johannes et al. (1999), based on their sampling, found peak numbers to occur sometime between 2 and 6 days before the new moon (BNM), but that the peak day might occur at any time within that period. While Golbuu and Friedlander (2011) indicated they did surveys during this period 2e6 days BNM, they evidently surveyed only once a month (a single day that was not specified) during that period. Numbers of fish have been documented to vary as much as 2e3 fold by Johannes et al. (1999) and up to 10 fold from our work between different days in the 2e6 day BNM period (Fig. 3). Results from other surveys (Johannes et al., 1999; PCS/ SCRFA, 2010) indicate it is necessary to sample at a minimum three days per lunar cycle (i.e. days 4 to 2 prior to the new moon to account for month to month and year to year variability). The highest density of any single survey rectangle at Ngerumekaol in 2005 relative to new moon is shown in Fig. 3 (data from Colin and Donaldson, in preparation). These data are quite similar to those of Johannes et al. (1999, Fig. 2) for numbers of fish counted on their surveys, and provide some confidence that the time of maximum aggregation size has not changed substantially for that site. Indeed, the maximum density of Epinephelus polyphekadion in 2005 was several times higher than that of the other two species, a result consistent with the much higher numbers of E. polyphekadion counted compared to other species by Johannes et al. (1999) in 1995e1996. The PCS/SCRFA (2010) surveys at Ebiil show a different peak day may generally occur there compared to Ngerumekaol, something that was also noted by Johannes et al. (1999). Although the PCS/ SCRFA surveys were started up to six days BNM, the peak day may have already passed as after the first day of surveys (6 BNM) the numbers of fishes declined rapidly. This implies that the survey days (not specified, but indicated as starting no earlier than 6 days BNM) of Golbuu and Friedlander (2011) might also have missed the peak aggregation day to Ebiil adding additional uncertainty to their data. Ideally a rise and subsequent fall of fish numbers needs to be documented to verify the peak day has been determined. The
Fig. 3. Maximum densities of three species of groupers found in any survey area by GPS density survey method in the Ngerumekaol spawning aggregation during 2005 relative to time of full moon (data from Colin and Donaldson, in preparation).
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possible reasons for different peak days between sites include differences in tidal regimes between sites, migration patterns or some other factor. Since Golbuu and Friedlander (2011) did not identify the specific days when their surveys were conducted (just the range of 2e6 days BNM), nor the exact locations of transects, we cannot directly compare our GPS density data to their transect data. However, because our data are geo-located, it would be possible and informative to compare their transect density data with our data from the same geographic location for the same days. 3.3. The numbers of fishes and species composition of the spawning aggregation change over the spawning season While the exact locations of the five transects at each site were not specified by Golbuu and Friedlander (2011), the failure of the Ebiil transects to capture data for one species (Epinephelus polyphekadion), except for a single fish, which the PCS/SCRFA surveys found to be abundant at the site, verifies that the short transects did not begin to cover the site adequately. Ideally, transects should cross the entire width of the aggregation, from areas with no aggregated fishes evident, and across the center of the aggregation to the opposite side where fishes again cease to be observed (2011). We maintain that problems with the Golbuu and Friedlander (2011) study began with the selection of the locations and deployment of the five transects at each site. Were these transects five sections of a continuous line (as per the 200 m long earlier PCS transect e see PCS/SCRFA, 2010), or were there five separate transects located in different areas? How were the transects selected? PCS/SCRFA (2010) clearly showed that the 200 m transect used earlier at Ebiil was not representative of the aggregations in general and totally missed the aggregation site of E. polyphekadion (Fig. 2). This problem was identified in 2003 and the omission was rectified by PCS/SCRFA in 2008 by changing to the GPS density survey method and surveying the entire site based on knowledge of its full spatial extent. Johannes et al. (1999) tried to cover the entire area of aggregations on their surveys, but did not provide any measurements of fish abundance/area that would yield density values for fishes present in these aggregations. This lack of density data was noted by Golbuu and Friedlander (2011), and should have immediately cautioned them about comparing data between the previous study and theirs. Indeed, in their discussion Golbuu and Friedlander (2011) say that the “differences in sampling methodology between Johannes et al. (1999) study and the present one precludes direct density comparisons but differences in species proportions between these two periods show large-scale changes since the mid-1990s”. However, since the same areas were not surveyed and because species can be distributed differently, then species proportions cannot be compared either. While these authors indicated they had assistance from participants in the Johannes et al. (1999) surveys in verifying that they were surveying in the same area, the comparisons of areas were not sufficiently precise to be comparable. Their lack of Epinephelus polyphekadion at Ebiil, while previously abundant, should have been an indication that something was amiss; instead they mistakenly concluded that the species had undergone a drastic decline in abundance. Despite their statement that “the almost total disappearance of E. polyphekadion at Ebiil is unequivocal”, the species is still present in large numbers (PCS/SCRFA, 2010), but found slightly deeper and obviously outside of their survey area.
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having been known previously as grouper aggregation sites, but had been fished out at sometime in the past. Rebotel was reported as a former aggregation site by Noah Idechong, ex-chief of the Palau Division of Marine Resources, in Johannes et al. (1999:4), who indicated that the fish found at the site was primarily Plectropomus areolatus, and that the site was fished out in the 1970s. The second site was reported to Golbuu and Friedlander (2011) verbally without validation. Separately in a study of Palauan fish spawning aggregation sites based upon interviews with Palauan fishermen, neither of these localities was identified as being spawning aggregation sites (Sadovy de Mitcheson, 2007). 4.1. Problems with maps of sites Major problems exist with regard to the geomorphology maps for the aggregation and reference sites (Golbuu and Friedlander, 2011; Fig. 2), which are based on the National Oceanographic and Atmospheric habitat survey maps for Palau (Battista et al., 2007). 4.1.1. Ngebard/Ebiil aggregation site comparison The NOAA habitat maps for the Ngebard aggregation site (the location of the aggregation is presumed to be indicated by a small dot in Golbuu and Friedlander, 2011; Fig. 4) shows an area in the source image covered in cloud, identified as “unknown”, an appropriate descriptor of the area (Battista et al., 2007). When Golbuu and Friedlander (2011) show the same area in their Fig. 4, it is indicated as “sand”. The Ebiil site is also indicated (again by a single dot) to occur in an area of sand (no cloud in source image). Due to the depth of the Ebiil Channel (35 m), however, the bottom is not visible in the source image and should actually have been indicated as “unknown”. Because the Ebiil aggregation site is actually on the reef (and possibly the Ngebard site as indicated), the indication that the aggregation sites occur on “sand” is surprising and inconsistent with known spawning habitats for these species (Johannes et al., 1999, unpublished data). The NOAA habitat maps have a minimum mapping unit (MMU) of 0.4 ha (4000 m2 in area). Both the Ebiil and Ngerumekaol aggregation sites approach 10,000 m2 in area, in excess of the MMU, and should have been indicated as “reef” habitat on the maps. However, much of the Ebiil site (as well as Ngebard) was too deep to be classified and were properly indicated as “unknown”. Fig. 2 of Golbuu and Friedlander (2011) should have indicated these areas as reef bottom, given that the aggregation sites were far in excess of the minimum mapping unit and actual ground truth knowledge resulting from fish surveys at the sites would have indicated the error in classifying these as sand. Due to these, and potentially other errors, the accuracy and use of these maps for characterizing and comparing these sites is questionable. We believe the comparison between Ngebard and Ebiil is flawed. The Ebiil Channel mouth in the area with the aggregation is much wider and deeper than Ngebard (500 m wide 35 m deep versus 200 m wide 25 m deep). Ngebard was not indicated as “a former aggregation site” by Johannes et al. (1999), contrary to what was stated in Golbuu and Friedlander (2011). Ngebard is located 12 km north along the barrier reef from Ebiil channel, while a further 6.5 km north of Ngebard is another validated grouper aggregation site, the “Western Entrance”, reported by Johannes et al. (1999) that still had aggregations of all three groupers when surveyed on a single day in June 2009. Why Ngebard would come to be fished out while sites on either side of it continue to have spawning aggregations deserves an explanation.
4. Comparison between aggregation and reference sites The non-protected reference or ‘control’ sites chosen by Golbuu and Friedlander (2011), Rebotel and Ngebard, were described as
4.1.2. Ngerumekaol/Rebotel The comparison between the other two sites, Ngerumekaol and Rebotel, is similarly inappropriate. While Golbuu and Friedlander
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(2011) considered both to be “incomplete channels”, their geomorphology is actually quite different, something easily seen in a superficial examination of their Fig. 2. Unlike Ebiil and Ngebard, both these areas are sufficiently shallow that the entire bottom can be seen and characterized. The deep portion of Ngerumekaol is nearly 1.5 km in length and over 100 m wide, with depths up to 12e16 m (Colin, 2009: 98) and is a popular dive site for tourists due to its abundance of marine life. The inner lagoon end of the channel has shallow reef only a few meters deep, but still exchanges large amounts of water through it on changing tides (Colin, 2009; Fig. 3.26). On the other hand, Rebotel channel (which is shown at a different scale in their figure) is shallow at its mouth (about 3e6 m depth) with a sill only a short distance (100e150 m) inside that can barely pass a small boat, and as such it is very different from Ngerumekaol (and is of no interest to tourist divers). Using the name “false passage” Colin (2009, Fig. 3.3) considered it of such a small size that no data were provided on width and depth in a table detailing all channels and passages through the Palau barrier reef (Colin, 2009: 82).
no way to begin to validate the past status of something that no longer exists without multiple sources providing definitive oral information. If information obtained from abundance and distribution surveys of aggregation sites are intended to guide management decisions, then great caution is needed to be certain that methods used are adequately characterizing the aggregations as they exist and are repeatable by others with comparable results in the future.
5. Discussion
References
The results reported in Golbuu and Friedlander (2011) are not based on sound science and hence are not supportable and likely to be misleading. They are, most significantly, the outcome of a failing to use a method for surveying the aggregation sites that encompasses the entire aggregation in a way that provides both distribution and density information either for individual species or for all the aggregating species of interest. The use of a limited number of short transects, the densities and proportions from them, in unknown sections of the aggregation sites does not begin to capture adequately the data necessary to characterize large spawning aggregations of three species that have somewhat different, but partially overlapping distributions and where each species is distributed unevenly within its own aggregation. The limited number of transects, particularly if they are in a continuous line, used by Golbuu and Friedlander (2011) almost guarantees that some portions of the aggregations will be missed or, at best, poorly sampled. The errors in the length and location of the transects caused the near total exclusion of one common species at one site from their data, which subsequently seriously biased results which were misinterpreted to mean that this species had undergone a disastrous decline in the numbers at that site and hence that management had been ineffective. Additional unknown, but potentially significant, errors in data collection were based on not sampling enough (ideally all) days 2e6 days before the new moon each month to identify when the day of peak abundance occurs. Our data indicate it is likely (as Johannes et al., 1999 suggested) that that peak abundance, relative to the new moon, may differ at different aggregation sites. To sample for the peak aggregation day at even a single site requires multiple days of data collection and to adequately sample among multiple sites involves many days of simultaneous sampling at two or more sites. Finally, the attempts to link spawning aggregation persistence with protected versus overexploited (“reference”) sites immediately falls short in that equivalent protected and “reference” sites are not available. The reference sites chosen as “controls” have many deficiencies for comparative purposes and it would have probably been better to just delete this component in the paper. We are proponents of the use of TEK in addressing fisheries management questions, however, such information should not be used to formulate policy without validation (Hamilton et al., 2011). To compare existing against virtually undocumented extirpated aggregations, the level of TEK needed is perhaps greater as there is
Acknowledgments GPS density transect surveys at Ngerumekaol in 2005 were made possible by a grant from The Nature Conservancy East Asia program. Other work by the senior author was supported by the Coral Reef Research Foundation. Surveys at Ebiil Channel were supported by a grant from the David and Lucille Packard Foundation to SCRFA and in collaboration with the Palau Conservation Society.
Battista, T.A., Costa, B.M., Anderson, S.L., 2007. Shallow-water Benthic Habitats of the Republic of Palau (DCD) NOAA Technical Memorandum NOS NCCOS 59, Biogeography Branch, Silver Spring, MD. Colin, P.L., 2011. Studying and monitoring aggregating species. In: de Mitcheson, Y.S., Colin, P.L. (Eds.), Reef Fish Spawning Aggregations: Biology, Research and Management. Fish & Fisheries Series, vol. 35. doi:10.1007/978-94007-1980-4_9. Colin, P.L., 2009. Marine Environments of Palau. Mutual Publishing, Honolulu, 414 pp. Colin, P.L., Sadovy, Y.J., Domeier, M.L., 2003. Manual for the Study and Conservation of Reef Fish Spawning Aggregations. In: Society for the Conservation of Reef Fish Aggregations Special Publication No. 1 (Version 1.0), pp. 98. Colin, P.L., Donaldson, T.J. Dynamics of grouper spawning aggregations in Palau. 2003e2006, in preparation. Colin, P.L., Donaldson, T.J., Martin, L.E. 2005. GPS density surveys: a new method for quantitatively assessing reef fish spawning aggregations (and other populations of reef fishes) (Abs.). In: Seventh Indo-Pacific Fish Conference, Taipei. Domeier, M.L., Colin, P.L., 1997. Tropical reef fish spawning aggregations: defined and reviewed. Bulletin of Marine Science 60 (3), 698e726. Golbuu, Y., Friedlander, A., 2011. Spatial and temporal characteristics of grouper spawning aggregations in marine protected areas in Palau, western Micronesia. Estuarine, Coastal and Shelf Science 92 (2), 223e231. Hamilton, R., Sadovy de Mitcheson, Y., Aguilar-Perera, A., 2011. The role of local ecological knowledge in the conservation and management of reef fish spawning aggregations. In: Sadovy de Mitcheson, Y., Colin, P.L. (Eds.), Reef Fish Spawning Aggregations: Biology, Research and Management. Springer. Johannes, R.E., 1981. Words of the Lagoon. University of California Press, Berkeley and Los Angeles, 245 pp. Johannes, R.E., Squire, L., Graham, T., Sadovy, Y., Renguul, H., 1999. Spawning Aggregations of Groupers (Serranidae) in Palau. In: The Nature Conservancy Marine Research Series Publication No. 1, 144 pp. Nemeth, R.S., Blondeau, J., Herzlieb, S., Kadison, E., 2007. Spatial and temporal patterns of movement and migration at spawning aggregations of red hind, Epinephelus guttatus, in the U.S. Virgin Islands. Environmental Biology of Fishes 78, 365e381. PCS/SCRFA, 2010. Enhanced Monitoring of Grouper Spawning Aggregation at Ebiil Channel: Final Technical Report, Palau Conservation Society and Society for the Conservation of Reef Fish Aggregations report, 31 pp. Available at: SCRFA.org/ news. Rhodes, K.L., Sadovy, Y., 2002. Reproduction in the camouflage grouper Epinephelus polyphekadion (Pisces: Serranidae) in Pohnpei, Federated states of Micronesia. Bulletin of Marine Science 70, 851e869. Sadovy, Y., 2005. Troubled times for the trysting trio: three aggregating groupers in the live reef fish-food trade. SPC Live Reef Fish Information Bulletin 14, 3e6. Sadovy, Y., Eklund, A.M., 1999. Synopsis of Biological Information on the Nassau Grouper, Epinephelus striatus (Bloch, 1792), and the Jewfish, E. itajara (Lichtenstein, 1822). NOAA Technical Report NMFS 146. Technical Report of the Fishery Bulletin. FAO Fisheries Synopsis 157. US Department of Commerce, Seattle, Washington. Sadovy de Mitcheson, Y., 2007. Report on Current Status and Exploitation History of Reef Fish Spawning Aggregations in Palau. In: Western Pacific Fishery Survey Series: Society for the Conservation of Reef Fish Aggregations, vol. 3. SCRFA and the Palau Conservation Society. Samoilys, M., 1997. Periodicity of spawning aggregations of coral trout Plectropomus leopardus (Pisces: Serranidae) on the northern Great Barrier Reef. Marine Ecology Progress Series 160, 149e159.
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Grouper spawning aggregations: Be careful what you measure and how you measure it: A rebuttal of Golbuu and Friedlander (2011) Patrick L. Colin a, *, Yvonne Sadovy de Mitcheson b, Terry J. Donaldson c a
Coral Reef Research Foundation, P.O. Box 1765, Koror, PW 96940, Palau School of Biological Sciences, University of Hong Kong, Puk Fu Lam Road, Hong Kong c University of Guam Marine Laboratory, UOG Station, Mangilao, GU 96923, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 May 2011 Accepted 13 October 2011 Available online 2 November 2011
Golbuu and Friedlander (2011, Estuar. Coast. Shelf Sci. 92:223) used faulty methods, improper interpretation of historical data, and assumptions of little or no validity to conclude that despite protected status spawning aggregations of three groupers in Palau, western Caroline Islands declined between 1995e96 and 2005e06. Alternate survey methods indicated no drastic declines in these aggregations over the same period. Golbuu and Friedlander (2011) failed to document the overall distribution of fishes in their aggregations, used poorly-located inadequate transects to sample the overall aggregation area, and did not identify and sample peak aggregations days. The use of visual length estimates as the basis for biomass values may introduce errors. Comparison of aggregation persistence between reference (“fished out”) and protected sites is not possible because equivalent protected and exploited sites are not available. Different species at multi-species spawning aggregation sites commonly occupy somewhat discrete locations, with the densest concentrations (core areas) of one often being separated from those for another. There is usually a single peak day each month of a lunar-based aggregation, but it requires multiple days data collection to determine that peak. The shortcomings identified provide important lessons for the study of fish spawning aggregations and signal caution about the incomplete documentation of sampling methodology. Overly simplistic aggregation sampling methodologies may be superficially credible, but are not reflective of a complicated reality. Monitoring needs to produce a definitive repeatable baseline against which data can be gathered authoritatively in the future. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: spawning aggregation grouper Palau survey methods traditional ecological knowledge conservation
1. Introduction In a recent paper in this journal, Golbuu and Friedlander (2011) presented data regarding the density and distribution/abundance of three species groupers (Pisces: Serranidae) at spawning aggregations in the Republic of Palau in the western Caroline Islands. Based on their data they concluded that, despite protections of various types, populations of these groupers underwent declines in numbers of fishes aggregating at two sites in 2005e2006 compared to a decade earlier (1995e1996) based on the unpublished report of Johannes et al. (1999) for the same sites. Unfortunately we must reject the conclusions of Golbuu and Friedlander (2011) as they are based upon faulty methods for monitoring fish spawning aggregations, improper interpretation of historical grouper data, and numerous assumptions of little or no validity. We believe that their
* Corresponding author. E-mail address: [email protected] (P.L. Colin). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.10.011
results, therefore, cannot be used to conclude anything about the status of these aggregations in Palau. The three grouper species (brown-marbled grouper e Epinephelus fuscoguttatus, camouflage grouper e Epinephelus polyphekadion and squaretail coralgrouper e Plectropomus areolatus) are often found aggregating at the same locations and times. These are “transient aggregations” (Domeier and Colin, 1997), meaning that fish engage in movements from home territories and remain at the aggregation site for a period of some days, usually on a lunar and seasonal basis. These spawning aggregations are the only time that these species, which support important fisheries at nonaggregation times, are known to reproduce and have variously received protection in the last two decades. Hence, using scientifically credible methods for the assessment of their status is important for understanding fisheries, and the effectiveness of management interventions. Spawning aggregations of these three species have been known in Palau historically as traditional ecological knowledge (TEK) that had been documented by Johannes et al. (1999) and Johannes (1981). Their unpublished
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report forms the starting point for evaluation of population changes by Golbuu and Friedlander (2011). 2. What are the problems? The monitoring of spawning aggregations for fish abundance and densities is challenging and depends on applying a welldesigned sampling protocol that is representative, clear and replicable. The Society for the Conservation of Reef Fish Aggregations (SCRFA) has made efforts to promote appropriate and repeatable methods for quantifying fish spawning aggregations. Spawning aggregations of groupers are quite variable in time and space within single sites and between multiple sites, thus it is critical to develop a sampling protocol with the appropriate time period, spatial coverage and sampling methodology, especially for multispecies aggregations (Colin et al., 2003; Colin, 2011). In the past few years work has been undertaken by SCRFA with the Palau Conservation Society (PCS) to better quantify grouper spawning aggregations in the Republic of Palau with some success (PCS/ SCRFA, 2010), including at one of the two sites (Ebiil) reported in Golbuu and Friedlander (2011) study. In addition, two of us (PCL and TJD) have used similar survey techniques at the second aggregation site (Ngerumekaol) from 2003 to 2010, with particularly intensive survey work in 2005 (Colin et al., 2005). The first step in planning any sampling regime for aggregation fish density and abundance, as well as to ensure replicability, is to determine the limits and general distribution of the aggregated fish(es). Within the aggregation area, numbers and density of fish, sex ratios, and size of individuals can change within a single day, between days, among lunar months, and on a seasonal basis. Appropriate and consistent sampling protocols should be used to make meaningful comparisons across time at any aggregation site. Isolated densities of fish(es) within an aggregation cannot be used as a meaningful measure of abundance if they vary across aggregation sites. Typically species have areas of higher density toward the center of the aggregation (core) and lower densities at the edges (Samoilys, 1997; Rhodes and Sadovy, 2002; Nemeth et al., 2007), and this is known for the groupers presently under consideration Therefore, fish numbers are best reported in terms of abundances, ideally based on a series of density measurements encompassing most to all of the aggregation. We question the methods and analysis of Golbuu and Friedlander (2011) to characterize the abundance of three groupers at the two study aggregation sites, then to draw conclusions regarding changes in aggregation numbers and hence the effectiveness (positive or negative) of management relative to the earlier study at the same sites. Additionally we doubt the study in question can be replicated, as the methods, locations and sampling times used are not adequately described. We believe also that the shortcomings of this research provide very important lessons in relation to the study of aggregations in general that cannot be ignored, as well as signal caution about the incomplete documentation of sampling methodology. We base our concerns primarily on an evaluation of the methodology provided by Golbuu and Friedlander (2011) and with support from results from other studies at the research sites involved (Johannes et al., 1999; Colin et al., 2005; Colin and Donaldson, in preparation; PCS/SCRFA, 2010), as well as on the same species elsewhere (Rhodes and Sadovy, 2002; Sadovy, 2005). Concerns arising from the study of Golbuu and Friedlander (2011) fall into seven areas; specifically:: (a) the use of isolated density as a measure of aggregation size and abundance; (b) the lack of specific details on the placement of transects relative to the total aggregation area implying an inability to meaningfully document either density or abundance; (c) the lack of replicability; (d)
the methods used to assess body size to evaluate changes between the present and past studies; (e) the use of a single day each month for sampling; (f) the overall conclusions regarding changes in aggregation status (compared with the Johannes et al., 1999), as well as comparison with “reference” sites; (g) conclusion that there was an unequivocal loss of camouflage grouper from the Ebiil site. 3. Measurement of aggregation size, fish numbers and density within aggregations, placement of transects and concerns about replicability Golbuu and Friedlander (2011) reported on surveys of two grouper aggregation sites in barrier reef channels, Ebiil and Ngerumekaol (also known as “Ulong Channel”), plus two reported former aggregation sites (called “reference areas”), Ngebard and Rebotel, monthly for 18 months. They indicate “surveys were conducted once a month, sometime 2e6 days before the new moon, which coincides with peak in aggregation density of several grouper species in Palau”, but did not identify any specific days before new moon (BNM) when surveys were conducted. We interpret this to mean transect surveys were done only on one day each month during that 2e6 days BNM period. Johannes et al. (1999) reported for each lunar month a peak in the number of fishes to aggregate on a single day sometime within this period, 2e6 days BNM, but the peak day was unpredictable. Golbuu and Friedlander (2011) surveyed five 50 5 m permanent transects (250 m2 each) at an unspecified depth at each site for the numbers of groupers, plus an assortment of other fishes. The locations and relationships of the transects were not provided. Sizes of fishes were estimated visually and estimates of total biomass of each species obtained from these estimated lengths using the lengtheweight relationships appearing in FishBase (fishbase.org). Golbuu and Friedlander (2011) did not elaborate further on how the transect sites were chosen, whether they were in a continuous line or separated from one another nor their relationship to the total area of aggregation of the three species. Three major problems stem from the inability of the five relatively short transects at each site, particularly if they are in a single line, to capture adequately the distribution and density of fishes that vary spatially both within and between species. Moreover, because Golbuu and Friedlander (2011) did not delimit the outer boundaries of the aggregation sites for the three study species, the placement of transects relative to their distributions or core areas is unknown. First, those authors state that placement of their five transects were in the same general locations as in the earlier Johannes et al. (1999) study. However, in Johannes et al. (1999) (one of the co-authors of which was YS) a core area for monitoring was simply delineated to include the largest proportion of the aggregation that it was possible to count on a dive with a single SCUBA tank by one person. This was an unknown proportion of the total aggregation and consisted mainly of Plectropomus areolatus, with Epinephelus polyphekadion less thoroughly covered because these fish were too deep to monitor fully. Second, Johannes et al. (1999) conducted a zigzag survey (not on a particular line) between rebar markers at the Ebiil site rather than a specific transect. Specific transects were also not indicated for Ngerumekaol, just that numbers of fish were monitored both in the channel and in the northern area near the channel mouth. Third, by limiting sampling to (apparently) one day per month for each aggregation it is uncertain whether the day of peak fish abundance (density) was sampled and this prevents valid comparisons between months and years. Although peak densities have been known to occur sometime within the period 2e6 days BNM, it is not consistent which day that is from month to month or between aggregation sites. It should be noted also that density in a small area is not necessarily proportional to total fish numbers.
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Golbuu and Friedlander (2011) sampled an unknown proportion of their study aggregations on a day of unknown relationship to peak densities for the month/year of study. This undoubtedly resulted in biased and flawed data that formed the basis for invalid conclusions and overall their surveys are not, given the present information, replicable by others. Short transects relative to the overall aggregation area for the study species are not recommended as a method of monitoring aggregation fishes (Colin et al., 2003), particularly for multi-species aggregations when the overall distribution of fishes is not known. The short transect methods used by Golbuu and Friedlander (2011) were not directly comparable to the earlier Johannes et al. (1999) study in survey pattern, placement or dimension. In general such short transect methods are not suitable for surveying fish spawning aggregations because their numbers, size and placement are critical. The densities of fishes within only a small portion of an aggregation cannot be used reliably for obtaining representative samples as a measure of total abundance, as fish density varies across the aggregation and decreases toward the edges of an aggregation. This is particularly true for multi-species aggregation, such as those of concern here, as different species have somewhat different distributions within an overall site. Also the overall area an aggregation occupies decreases with lower total fish numbers. During a large aggregation those areas outside the core of the aggregation would have densities lower than those of fish in the core, but during an aggregation with fewer fish (and a smaller overall area) these same areas might totally lack fish, although densities of fish are still high in the core area. We also believe the use of visual length estimates as the basis for biomass values may introduce substantial errors at multiple levels, but that cannot be determined. The conversion of estimated length of groupers to biomass is further complicated with fish present in spawning aggregations are generally larger individuals with considerable variation in body weight (as much as 2 times) for a given length (for example see Sadovy and Eklund, 1999), hence using estimated length to determine biomass of a group of fishes is dubious, and accuracy of data unknown. More appropriate (but still with inherent errors) would have been the comparison of size frequency histograms at 5 cm intervals for Plectropomus areolatus with those of Johannes et al. (1999), but this was not done. The use of uncertain biomass values rather than fish abundance also fails to describe adequately the characteristics of a spawning aggregation. Even if length and consequently weight data were accurate, a few large, heavy fish might comprise a given aggregation but the actual size of the aggregation would be smaller compared to one with many smaller but reproductively active fish; this distinction has consequences for determining both population size and the overall reproductive potential of the aggregation, especially if sex-specific body sizes (e.g., males larger than females) and sex ratios are skewed.
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site (more on this subject below), yet there are also large areas that have either a single species present, or the others at very low densities (Fig. 1). The outer limits were determined by using GPS surveys (Colin et al., 2005; Colin, 2011) to delineate boundaries beyond which groupers ceased to occur (PCS/SCRFA, 2010). The density of fish within the aggregation increases toward its central area (Fig. 2) and a few short transects placed haphazardly within the overall aggregation area will almost certainly produce a highly biased sampling of fish numbers. In a worst case, a species may be totally missed by poor selection of transects locations, such as that of the original PCS transect (Fig. 2) and presumably the Golbuu and Friedlander (2011) transect locations. In addition to the problem of differing overall distributions for species, the density of a single species within an aggregation differs and decreases from a central (i.e. core) area to zero at the edges of the aggregation (Fig. 2). To measure the highest density within an aggregation on any given day it is necessary to know where that location is, otherwise measuring density on short transects does not provide an estimate of total numbers or biomass within an aggregation. Data from GPS density surveys indicate that the same location is not always the area of highest density on different days. Interestingly, the role of geomorphology in individual species distributions is well illustrated in Fig. 1. At Ebiil (Fig. 1a) the three
3.1. Different grouper species tend to occupy different areas within spawning aggregation sites Different fish species at multi-species spawning aggregation sites commonly occupy somewhat discrete locations, with the densest concentrations (core areas) of one species often being separated from such areas for another. Within a multi-species site, the overall distribution of a species, however, often overlaps into aggregation areas of another species to the point so that the multiple species form a continuous area occupied by one or more species. This is typical for the three grouper species that form spawning aggregations at the two active Palau spawning aggregation sites, especially Ebiil (Colin et al., 2003, 2005; PCS/SCRFA, 2010). There are areas of overlap, particularly at the Ngerumekaol
Fig. 1. Geographic limits of spawning aggregations of three grouper species typical of days of peak aggregation at (a) Ebiil channel, and (b) Ngerumekaol channel, Palau. Areas were surveyed with the GPS density method and limits shown are based on surveys conducted on a single peak day in 2009 for Ebiil (PCS/SCRFA, 2010) and in 2005 for Ngerumekaol (Colin and Donaldson, unpublished data). The location of transects of Golbuu and Friedlander (2011) within these areas are not known, however the scale distance scale shown for both areas is divided into 50 m increments to indicate the relative length of 50 m transects compared to the overall distribution of fishes.
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3.2. The peak day of aggregation varies and it is necessary to survey multiple days to determine peak day
Fig. 2. Example of a GPS density bubble plot for Epinephelus polyphekadion during a peak spawning day at Ebiil Channel, Palau showing the decrease in density away from the central “core” area and outer limits of the aggregation. Empty circles are areas with no fish. The location of the original Palau Conservation Society transect (200 m in length) is shown to indicate how a species would be missed by a poorly placed short transect.
groupers occur along the southern reef slope at the mouth of the channel with the bathymetry indicated. These groupers have been reported to have formed spawning aggregations previously along the north-side slope, but they no longer do so (Johannes et al., 1999). The channel mouth reaches at least 35 m in depth, becoming sandy on the middle flat section, and the groupers occur only along the reef-covered slope and do not go below ca. 30 m. When numbers of individual fishes are high (Fig. 1a), the distributions of the three species overlap somewhat. When fish numbers are lower, the overlap is minimal or does not exist, with the aggregation of each species centered on the core area of its individual distribution. This can be seen in the overall PCS/SCRFA Ebiil data (PCS/SCRFA, 2010, Figs. 5 and 11). At Ngerumekaol, the channel is shallower, with lush reef generally about 9e12 m in depth across the channel mouth, with sides or walls that slope steeply upward to a reef flat only 1e2 m deep. The aggregation area includes both sides of the channel as well as the central bottom area (Fig. 1b). While the three species still have somewhat different distributions that are maintained throughout the aggregation season, there is more overlap in their occurrence compared to Ebiil. The distribution of Epinephelus fuscoguttatus is centered on the channel bottom area about 200e300 m inside the mouth and fish are not common up the channel sides. The highest densities of the other two species are found both on the channel bottom and also up the sides of the channel, however, the population of E. polyphekadion is located closer to the channel mouth, while Plectropomus areolatus extends much further into the channel. If even higher numbers of fishes were present, these relative distributions might change. Johannes et al. (1999) clearly encountered all three species of groupers at the Ebiil site and the data they presented on relative abundance for 1995e1996 (Epinephelus fuscoguttatus e 21e19%, Epinephelus polyphekadion e 43e52%, Plectropomus areolatus e 3528%) indicate all species are common in the aggregations. Johannes et al. (1999) conducted surveys down to 35 m depth and as such would have encountered the deeper E. polyphekadion aggregation missed by Golbuu and Friedlander (2011). Indeed, they reported maximal counts of E. polyphekadion at Ebiil of over 900 fish.
Knowledge of exactly when the numbers of fish within an aggregation for each species peaks before the new moon is imperfect. Johannes et al. (1999), based on their sampling, found peak numbers to occur sometime between 2 and 6 days before the new moon (BNM), but that the peak day might occur at any time within that period. While Golbuu and Friedlander (2011) indicated they did surveys during this period 2e6 days BNM, they evidently surveyed only once a month (a single day that was not specified) during that period. Numbers of fish have been documented to vary as much as 2e3 fold by Johannes et al. (1999) and up to 10 fold from our work between different days in the 2e6 day BNM period (Fig. 3). Results from other surveys (Johannes et al., 1999; PCS/ SCRFA, 2010) indicate it is necessary to sample at a minimum three days per lunar cycle (i.e. days 4 to 2 prior to the new moon to account for month to month and year to year variability). The highest density of any single survey rectangle at Ngerumekaol in 2005 relative to new moon is shown in Fig. 3 (data from Colin and Donaldson, in preparation). These data are quite similar to those of Johannes et al. (1999, Fig. 2) for numbers of fish counted on their surveys, and provide some confidence that the time of maximum aggregation size has not changed substantially for that site. Indeed, the maximum density of Epinephelus polyphekadion in 2005 was several times higher than that of the other two species, a result consistent with the much higher numbers of E. polyphekadion counted compared to other species by Johannes et al. (1999) in 1995e1996. The PCS/SCRFA (2010) surveys at Ebiil show a different peak day may generally occur there compared to Ngerumekaol, something that was also noted by Johannes et al. (1999). Although the PCS/ SCRFA surveys were started up to six days BNM, the peak day may have already passed as after the first day of surveys (6 BNM) the numbers of fishes declined rapidly. This implies that the survey days (not specified, but indicated as starting no earlier than 6 days BNM) of Golbuu and Friedlander (2011) might also have missed the peak aggregation day to Ebiil adding additional uncertainty to their data. Ideally a rise and subsequent fall of fish numbers needs to be documented to verify the peak day has been determined. The
Fig. 3. Maximum densities of three species of groupers found in any survey area by GPS density survey method in the Ngerumekaol spawning aggregation during 2005 relative to time of full moon (data from Colin and Donaldson, in preparation).
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possible reasons for different peak days between sites include differences in tidal regimes between sites, migration patterns or some other factor. Since Golbuu and Friedlander (2011) did not identify the specific days when their surveys were conducted (just the range of 2e6 days BNM), nor the exact locations of transects, we cannot directly compare our GPS density data to their transect data. However, because our data are geo-located, it would be possible and informative to compare their transect density data with our data from the same geographic location for the same days. 3.3. The numbers of fishes and species composition of the spawning aggregation change over the spawning season While the exact locations of the five transects at each site were not specified by Golbuu and Friedlander (2011), the failure of the Ebiil transects to capture data for one species (Epinephelus polyphekadion), except for a single fish, which the PCS/SCRFA surveys found to be abundant at the site, verifies that the short transects did not begin to cover the site adequately. Ideally, transects should cross the entire width of the aggregation, from areas with no aggregated fishes evident, and across the center of the aggregation to the opposite side where fishes again cease to be observed (2011). We maintain that problems with the Golbuu and Friedlander (2011) study began with the selection of the locations and deployment of the five transects at each site. Were these transects five sections of a continuous line (as per the 200 m long earlier PCS transect e see PCS/SCRFA, 2010), or were there five separate transects located in different areas? How were the transects selected? PCS/SCRFA (2010) clearly showed that the 200 m transect used earlier at Ebiil was not representative of the aggregations in general and totally missed the aggregation site of E. polyphekadion (Fig. 2). This problem was identified in 2003 and the omission was rectified by PCS/SCRFA in 2008 by changing to the GPS density survey method and surveying the entire site based on knowledge of its full spatial extent. Johannes et al. (1999) tried to cover the entire area of aggregations on their surveys, but did not provide any measurements of fish abundance/area that would yield density values for fishes present in these aggregations. This lack of density data was noted by Golbuu and Friedlander (2011), and should have immediately cautioned them about comparing data between the previous study and theirs. Indeed, in their discussion Golbuu and Friedlander (2011) say that the “differences in sampling methodology between Johannes et al. (1999) study and the present one precludes direct density comparisons but differences in species proportions between these two periods show large-scale changes since the mid-1990s”. However, since the same areas were not surveyed and because species can be distributed differently, then species proportions cannot be compared either. While these authors indicated they had assistance from participants in the Johannes et al. (1999) surveys in verifying that they were surveying in the same area, the comparisons of areas were not sufficiently precise to be comparable. Their lack of Epinephelus polyphekadion at Ebiil, while previously abundant, should have been an indication that something was amiss; instead they mistakenly concluded that the species had undergone a drastic decline in abundance. Despite their statement that “the almost total disappearance of E. polyphekadion at Ebiil is unequivocal”, the species is still present in large numbers (PCS/SCRFA, 2010), but found slightly deeper and obviously outside of their survey area.
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having been known previously as grouper aggregation sites, but had been fished out at sometime in the past. Rebotel was reported as a former aggregation site by Noah Idechong, ex-chief of the Palau Division of Marine Resources, in Johannes et al. (1999:4), who indicated that the fish found at the site was primarily Plectropomus areolatus, and that the site was fished out in the 1970s. The second site was reported to Golbuu and Friedlander (2011) verbally without validation. Separately in a study of Palauan fish spawning aggregation sites based upon interviews with Palauan fishermen, neither of these localities was identified as being spawning aggregation sites (Sadovy de Mitcheson, 2007). 4.1. Problems with maps of sites Major problems exist with regard to the geomorphology maps for the aggregation and reference sites (Golbuu and Friedlander, 2011; Fig. 2), which are based on the National Oceanographic and Atmospheric habitat survey maps for Palau (Battista et al., 2007). 4.1.1. Ngebard/Ebiil aggregation site comparison The NOAA habitat maps for the Ngebard aggregation site (the location of the aggregation is presumed to be indicated by a small dot in Golbuu and Friedlander, 2011; Fig. 4) shows an area in the source image covered in cloud, identified as “unknown”, an appropriate descriptor of the area (Battista et al., 2007). When Golbuu and Friedlander (2011) show the same area in their Fig. 4, it is indicated as “sand”. The Ebiil site is also indicated (again by a single dot) to occur in an area of sand (no cloud in source image). Due to the depth of the Ebiil Channel (35 m), however, the bottom is not visible in the source image and should actually have been indicated as “unknown”. Because the Ebiil aggregation site is actually on the reef (and possibly the Ngebard site as indicated), the indication that the aggregation sites occur on “sand” is surprising and inconsistent with known spawning habitats for these species (Johannes et al., 1999, unpublished data). The NOAA habitat maps have a minimum mapping unit (MMU) of 0.4 ha (4000 m2 in area). Both the Ebiil and Ngerumekaol aggregation sites approach 10,000 m2 in area, in excess of the MMU, and should have been indicated as “reef” habitat on the maps. However, much of the Ebiil site (as well as Ngebard) was too deep to be classified and were properly indicated as “unknown”. Fig. 2 of Golbuu and Friedlander (2011) should have indicated these areas as reef bottom, given that the aggregation sites were far in excess of the minimum mapping unit and actual ground truth knowledge resulting from fish surveys at the sites would have indicated the error in classifying these as sand. Due to these, and potentially other errors, the accuracy and use of these maps for characterizing and comparing these sites is questionable. We believe the comparison between Ngebard and Ebiil is flawed. The Ebiil Channel mouth in the area with the aggregation is much wider and deeper than Ngebard (500 m wide 35 m deep versus 200 m wide 25 m deep). Ngebard was not indicated as “a former aggregation site” by Johannes et al. (1999), contrary to what was stated in Golbuu and Friedlander (2011). Ngebard is located 12 km north along the barrier reef from Ebiil channel, while a further 6.5 km north of Ngebard is another validated grouper aggregation site, the “Western Entrance”, reported by Johannes et al. (1999) that still had aggregations of all three groupers when surveyed on a single day in June 2009. Why Ngebard would come to be fished out while sites on either side of it continue to have spawning aggregations deserves an explanation.
4. Comparison between aggregation and reference sites The non-protected reference or ‘control’ sites chosen by Golbuu and Friedlander (2011), Rebotel and Ngebard, were described as
4.1.2. Ngerumekaol/Rebotel The comparison between the other two sites, Ngerumekaol and Rebotel, is similarly inappropriate. While Golbuu and Friedlander
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(2011) considered both to be “incomplete channels”, their geomorphology is actually quite different, something easily seen in a superficial examination of their Fig. 2. Unlike Ebiil and Ngebard, both these areas are sufficiently shallow that the entire bottom can be seen and characterized. The deep portion of Ngerumekaol is nearly 1.5 km in length and over 100 m wide, with depths up to 12e16 m (Colin, 2009: 98) and is a popular dive site for tourists due to its abundance of marine life. The inner lagoon end of the channel has shallow reef only a few meters deep, but still exchanges large amounts of water through it on changing tides (Colin, 2009; Fig. 3.26). On the other hand, Rebotel channel (which is shown at a different scale in their figure) is shallow at its mouth (about 3e6 m depth) with a sill only a short distance (100e150 m) inside that can barely pass a small boat, and as such it is very different from Ngerumekaol (and is of no interest to tourist divers). Using the name “false passage” Colin (2009, Fig. 3.3) considered it of such a small size that no data were provided on width and depth in a table detailing all channels and passages through the Palau barrier reef (Colin, 2009: 82).
no way to begin to validate the past status of something that no longer exists without multiple sources providing definitive oral information. If information obtained from abundance and distribution surveys of aggregation sites are intended to guide management decisions, then great caution is needed to be certain that methods used are adequately characterizing the aggregations as they exist and are repeatable by others with comparable results in the future.
5. Discussion
References
The results reported in Golbuu and Friedlander (2011) are not based on sound science and hence are not supportable and likely to be misleading. They are, most significantly, the outcome of a failing to use a method for surveying the aggregation sites that encompasses the entire aggregation in a way that provides both distribution and density information either for individual species or for all the aggregating species of interest. The use of a limited number of short transects, the densities and proportions from them, in unknown sections of the aggregation sites does not begin to capture adequately the data necessary to characterize large spawning aggregations of three species that have somewhat different, but partially overlapping distributions and where each species is distributed unevenly within its own aggregation. The limited number of transects, particularly if they are in a continuous line, used by Golbuu and Friedlander (2011) almost guarantees that some portions of the aggregations will be missed or, at best, poorly sampled. The errors in the length and location of the transects caused the near total exclusion of one common species at one site from their data, which subsequently seriously biased results which were misinterpreted to mean that this species had undergone a disastrous decline in the numbers at that site and hence that management had been ineffective. Additional unknown, but potentially significant, errors in data collection were based on not sampling enough (ideally all) days 2e6 days before the new moon each month to identify when the day of peak abundance occurs. Our data indicate it is likely (as Johannes et al., 1999 suggested) that that peak abundance, relative to the new moon, may differ at different aggregation sites. To sample for the peak aggregation day at even a single site requires multiple days of data collection and to adequately sample among multiple sites involves many days of simultaneous sampling at two or more sites. Finally, the attempts to link spawning aggregation persistence with protected versus overexploited (“reference”) sites immediately falls short in that equivalent protected and “reference” sites are not available. The reference sites chosen as “controls” have many deficiencies for comparative purposes and it would have probably been better to just delete this component in the paper. We are proponents of the use of TEK in addressing fisheries management questions, however, such information should not be used to formulate policy without validation (Hamilton et al., 2011). To compare existing against virtually undocumented extirpated aggregations, the level of TEK needed is perhaps greater as there is
Acknowledgments GPS density transect surveys at Ngerumekaol in 2005 were made possible by a grant from The Nature Conservancy East Asia program. Other work by the senior author was supported by the Coral Reef Research Foundation. Surveys at Ebiil Channel were supported by a grant from the David and Lucille Packard Foundation to SCRFA and in collaboration with the Palau Conservation Society.
Battista, T.A., Costa, B.M., Anderson, S.L., 2007. Shallow-water Benthic Habitats of the Republic of Palau (DCD) NOAA Technical Memorandum NOS NCCOS 59, Biogeography Branch, Silver Spring, MD. Colin, P.L., 2011. Studying and monitoring aggregating species. In: de Mitcheson, Y.S., Colin, P.L. (Eds.), Reef Fish Spawning Aggregations: Biology, Research and Management. Fish & Fisheries Series, vol. 35. doi:10.1007/978-94007-1980-4_9. Colin, P.L., 2009. Marine Environments of Palau. Mutual Publishing, Honolulu, 414 pp. Colin, P.L., Sadovy, Y.J., Domeier, M.L., 2003. Manual for the Study and Conservation of Reef Fish Spawning Aggregations. In: Society for the Conservation of Reef Fish Aggregations Special Publication No. 1 (Version 1.0), pp. 98. Colin, P.L., Donaldson, T.J. Dynamics of grouper spawning aggregations in Palau. 2003e2006, in preparation. Colin, P.L., Donaldson, T.J., Martin, L.E. 2005. GPS density surveys: a new method for quantitatively assessing reef fish spawning aggregations (and other populations of reef fishes) (Abs.). In: Seventh Indo-Pacific Fish Conference, Taipei. Domeier, M.L., Colin, P.L., 1997. Tropical reef fish spawning aggregations: defined and reviewed. Bulletin of Marine Science 60 (3), 698e726. Golbuu, Y., Friedlander, A., 2011. Spatial and temporal characteristics of grouper spawning aggregations in marine protected areas in Palau, western Micronesia. Estuarine, Coastal and Shelf Science 92 (2), 223e231. Hamilton, R., Sadovy de Mitcheson, Y., Aguilar-Perera, A., 2011. The role of local ecological knowledge in the conservation and management of reef fish spawning aggregations. In: Sadovy de Mitcheson, Y., Colin, P.L. (Eds.), Reef Fish Spawning Aggregations: Biology, Research and Management. Springer. Johannes, R.E., 1981. Words of the Lagoon. University of California Press, Berkeley and Los Angeles, 245 pp. Johannes, R.E., Squire, L., Graham, T., Sadovy, Y., Renguul, H., 1999. Spawning Aggregations of Groupers (Serranidae) in Palau. In: The Nature Conservancy Marine Research Series Publication No. 1, 144 pp. Nemeth, R.S., Blondeau, J., Herzlieb, S., Kadison, E., 2007. Spatial and temporal patterns of movement and migration at spawning aggregations of red hind, Epinephelus guttatus, in the U.S. Virgin Islands. Environmental Biology of Fishes 78, 365e381. PCS/SCRFA, 2010. Enhanced Monitoring of Grouper Spawning Aggregation at Ebiil Channel: Final Technical Report, Palau Conservation Society and Society for the Conservation of Reef Fish Aggregations report, 31 pp. Available at: SCRFA.org/ news. Rhodes, K.L., Sadovy, Y., 2002. Reproduction in the camouflage grouper Epinephelus polyphekadion (Pisces: Serranidae) in Pohnpei, Federated states of Micronesia. Bulletin of Marine Science 70, 851e869. Sadovy, Y., 2005. Troubled times for the trysting trio: three aggregating groupers in the live reef fish-food trade. SPC Live Reef Fish Information Bulletin 14, 3e6. Sadovy, Y., Eklund, A.M., 1999. Synopsis of Biological Information on the Nassau Grouper, Epinephelus striatus (Bloch, 1792), and the Jewfish, E. itajara (Lichtenstein, 1822). NOAA Technical Report NMFS 146. Technical Report of the Fishery Bulletin. FAO Fisheries Synopsis 157. US Department of Commerce, Seattle, Washington. Sadovy de Mitcheson, Y., 2007. Report on Current Status and Exploitation History of Reef Fish Spawning Aggregations in Palau. In: Western Pacific Fishery Survey Series: Society for the Conservation of Reef Fish Aggregations, vol. 3. SCRFA and the Palau Conservation Society. Samoilys, M., 1997. Periodicity of spawning aggregations of coral trout Plectropomus leopardus (Pisces: Serranidae) on the northern Great Barrier Reef. Marine Ecology Progress Series 160, 149e159.