Changes in the Spear Fishery of Herbivores Associated with Closed Grouper Season in Palau, Micronesia

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Animal Conservation. Print ISSN 1367-9430 Changes in the spear ﬁshery of herbivores associated with closed grouper season in Palau, Micronesia S. Bejarano Chavarro1, P. J. Mumby1 & Y. Golbuu2

1 Marine Spatial Ecology Lab, University of Queensland, St Lucia Campus, Brisbane, Qld, Australia 2 Palau International Coral Reef Center, Koror, Palau

Keywords Abstract coral reefs; herbivores; spearfishing; Micronesia; Palau; seasonal closures. Several species of coral reef herbivorous fish and groupers (Serranidae) are among the main targets of Micronesian spearfishers. Since 1994, a closed season (April– Correspondence July) protects spawning aggregations of five grouper species in Palau, and, Sonia Bejarano Chavarro, Central Caribbean although this regulation may affect fishers targeting behaviour towards herbivores Marine Institute, Little Cayman Research and increase their catch levels, the extent of these effects was previously unknown. Centre, North Coast Road, P.O. Box 37, This study conducted market surveys and interviews to examine if the closed Little Cayman KY3-2501, Cayman Islands. grouper season in 2009 had any effect on herbivore spearfishing catches, or caused Phone: (345) 948 1094 changes in the targeting behaviour of fishers. Catch volumes of the most desirable Email: [email protected] herbivores were unaffected by the grouper season, but the catch per unit effort of herbivores regularly caught opportunistically (i.e. if seen) or avoided raised by 45% Editor: Trevor Branch during the grouper closure. The size composition of the catch of the bluespine Associate Editor: Olaf Jensen unicornfish Naso unicornis during the grouper closure was significantly skewed to smaller sized fish due to the high proportion of immature individuals. Further Received 21 June 2012; accepted 10 June investigation is required to clarify whether this pattern emerged because fishers 2013 had relaxed size selectivity during the closure or due to a paucity of adults in July. Fifty-seven per cent of the interviewed fishers indicated that while groupers would doi:10.1111/acv.12066 be their first choice during open season, N. unicornis would become their preferred target during the closure, and that other herbivores were also more likely to be targeted. This study took an important step in identifying a factor driving short and acute changes in the herbivore catch composition. Further efforts should be directed to quantify the ecological implications of the observed changes and determine if these are aggravated by the life-history traits or functional roles of the focal species. Relaxed species selectivity might emerge elsewhere, if inherently selective fishing methods are used and highly prized targets are temporarily or permanently banned, or overfished to critical levels. Such implications should be considered when assessing the sustainability of local fisheries.

Introduction Friedlander, 1998; Graham & Idechong, 1998; Joseph, 2006; Bavnick et al., 2008). However, the effects of these restric- Artisanal fishing is practised as a primary source of food tions on the behaviour of fishers and the fishing pressure and economic income in many tropical coasts and develop- received by alternative species have rarely been investigated. ing nations around the world (Jennings & Polunin, 1996). In It is possible that fishers respond to restricted access to the tropical Pacific, spearfishing is a relatively affordable profitable species by switching to alternative targets. Such a and therefore widely distributed fishing method that focuses response is especially likely for fisheries that are highly selec- on exploiting coral reef fish (Dalzell, Adams & Polunin, tive with respect to species and size, such as spear fisheries 1996). With growing human populations leading to an (Frisch et al., 2008; Passley, Aiken & Perry, 2010). increased fishing intensity, several types of conservation Although it could be argued that any effect of a short- measures (e.g. gear restrictions, size limits, catch quotas and term closure on the catch of alternative species will only be seasonal closures) have been implemented to manage coral temporary, it might repeat every year, for as long as the reef fisheries (Cinner et al., 2006). Seasonal closures are closure remains effective, thus carrying a cumulative impact. among the most widely used fishing regulations, established Therefore, the implications of seasonal closures need to be to protect populations of commercially important species investigated and considered when assessing the sustainabil- during periods of reproduction (Johannes, 1978b; Beets & ity of local fisheries. Moreover, the changes in fishing

Animal Conservation 17 (2014) 133–143 © 2013 The Zoological Society of London 133 Spear fishery of herbivores during closed grouper season S. Bejarano Chavarro, P. J. Mumby and Y. Golbuu behaviour in response to seasonal restrictions on commercially important species might give insight into how fishers would respond to population depletions of the same. In Palau (Micronesia), as in several areas across the tropical Pacific, both groupers (Serranidae) and herbivores (i.e. parrotfishes, Scaridae; unicornfishes and surgeonfishes, Acanthuridae; rabbitfishes, Siganidae) are among the main targets of spearfishers (Dalzell et al., 1996; Rhodes & Tupper, 2007). Groupers are especially vulnerable to overfishing because of their slow growth, large size of maturity, and because they form spawning aggregations at pre- dictable locations and times (Johannes, 1981; Johannes et al., 1999). The loss of important grouper spawning aggregations in Palau in both the 1970s and the 1990s (Johannes et al., 1999) led to the establishment of a seasonal closure through the 1994 Marine Protection Act. Today, the law prohibits the possession and any form of commerce of five species of groupers, namely Epinephelus fuscoguttatus, E. polyphekadion, Plectropomus areolatus, P. laevis and P. leopardus, during the summer months of April through July, to protect them during their peak spawning aggregation period. It is reasonable to expect an increase in spearfishing pressure on herbivorous fish during the months of the grouper closure. In fact, this occurred in Pohnpei (Rhodes & Tupper, 2007). Collectively, herbivores provide the foundation for the grazing function in most Pacific reefs (Hoey & Bellwood, 2008), and species that fulfil particular functional roles within the guild (e.g. macroalgal browsing) are required to reverse the macroalgal dominance often established after disturbance (Hoey & Bellwood, 2009). As exploiting herbivores may compromise ecosystem function even before stocks are considered overfished (Mumby et al., 2012; Bejarano et al., in press), it is important to quantify the extent to which the grouper restriction affects herbivore catch volume and composition. In this study, we hypoth- esized that during the grouper closure, the catch of herbivores would increase in volume and would contain a higher proportion of small-bodied – generally undesirable – species that may contribute to the fishers’ profit. We tested this hypothesis by examining the differences in herbivore landings in Palau when the catch of groupers was restricted and when it was permitted. The effect of the grouper closure on the targeting behaviour of spearfishers was assessed through Figure 1 Map of the study area, Palau (Micronesia), indicating (with a individual interviews. star) the location of the surveyed market in Koror.

Materials and methods Dalzell, 1994). As a result, ordinances have been enacted that have banned scuba spearfishing, have regulated Study area minimum mesh size, have imposed season closures The Republic of Palau, with a population of 20 956 (United (Johannes, 1991) and have banned the harvest of Nations’ estimate 2011), is located 741 km east of the Phil- Bolbometopon muricatum permanently (Anonymous, 2007). ippines and 1300 km south-west of Guam (Fig. 1). Palau Eighty-seven per cent of Palauan households currently have has over 500 km2 of reefs, including a 144-km barrier along at least one member fishing for subsistence, for sale or both the West Coast, and a system of 10 marine-protected areas (Fitzpatrick & Donaldson, 2007). According to the latest spanning various reef habitats (Golbuu et al., 2005). South Pacific Forum Fisheries Agency report (Nichols, Palauan fishers have been concerned over diminishing 1991), seafood used to be landed mainly at the principal fish stocks of herbivores since the mid-1970s (Kitalong & market in Koror, but also at other five sites distributed

134 Animal Conservation 17 (2014) 133–143 © 2013 The Zoological Society of London S. Bejarano Chavarro, P. J. Mumby and Y. Golbuu Spear fishery of herbivores during closed grouper season across smaller villages. In 2009, the main fish market in Table 1 Commercially important (non-herbivore) species targeted by Koror remained the only active landing site where reef fish spearfishers in Palau, including the groupers protected by the were marketed daily. Being the main supplier of reef fish for April–July closure. Photocards of the species marked with an ‘×’in locals, restaurants and hotels, this market was the focus of the left column were presented to fishers (along with the favourite our field surveys (Fig. 1). herbivores) to assess their targeting behaviour during open grouper season. Photocards of all species (except the protected groupers) were presented to fishers to assess their change in preferences Field surveys during closed grouper season (right column)

Open grouper Grouper Market-based catch surveys Species season scenario closure scenario To examine the herbivore catch composition and volume, Plectropomus leopardus × daily surveys of reef fish landings at the Koror fish market Plectropomus laevis × were conducted over the last 2 weeks (18–31 March) of the Epinephelus fuscoguttatus × 8-month open grouper season (August–March), and the last Plectropomus areolatus × 2 weeks (13–26 July) of the 4-month grouper closure (April– Epinephelus polyphekadion × July) in 2009. Surveys were timed during new moon periods, Variola louti ×× when the fishing pressure on herbivorous fish is highest Variola albimarginata ×× ×× (Rhodes, Tupper & Wichilmel, 2008), and tailored to maxi- Cephalopholis argus ×× mize encounters with nocturnal spearfishers (i.e. 05:00– Epinephelus coeruleopunctatus ×× 10:00 h), who usually bring most herbivorous fish. All Lutjanus gibbus Lethrinus olivaceus ×× catches were landed directly at the market’s pier and imme- Lethrinus obsoletus ×× diately transferred to the store for sale. Although trading Lethrinus xanthochilus ×× started briskly after landing, the market staff ensured that Lutjanus monostigma ×× all catches (i.e. nclosed season = 19 and nopen season = 23) were surveyed prior to purchase. The catch landed by each boat was examined separately, and all parrotfish (Scaridae), surgeonfish and unicornfish (Acanthuridae), and rabbitfish (Siganidae) were identified to species, weighed to the nearest gram and measured to the nearest 0.1 cm for total length that reach similar sizes (refer to Bejarano et al., 2013 for (TL). Effort data were obtained by recording the number of further details on the interviewing protocol). These batches fishers associated to each catch and total time spent fishing were presented sequentially and in the same order to all (including travelling time). Most spearfishers used three- fishers asking them to assign each species a ‘decision’ among prong spears also known as Hawaiian slings, or rubber actively targeted, caught if seen but not looked for (oppor- spearguns. However, due to logistic constraints, the specific tunistically harvested), and avoided. Hypothesizing that all type of spearguns associated with each catch was not noted. species of interest were available and of an optimal size, Because Palauan fishers are reluctant to disclose any infor- fishers were then required to rank them in order of prefer- mation on the geographic origin of their catch, we abstained ence. At the end of each interview, the surveyor was able to from inquiring about their fishing locations. Therefore, we distinguish the most desirable species (actively targeted) were unable to assess the geographical extent of our catch from the least desirable ones (opportunistically harvested surveys. Fishers usually retained a small percentage of the and avoided), and the preferred species of each family (i.e. herbivore catch for personal consumption (<5%). Although Scaridae, Acanthuridae and Siganidae). this portion of the catch was often visually inspected, it To test whether the targeting behaviour towards herbi- could not be quantified consistently and was therefore vores is affected by the grouper closure, each fisher was excluded from the analyses. presented with two hypothetical scenarios. The first scenario recreated the open grouper season and required the fisher to rank (in order of preference) a new set of photocards that Interview-based assessment of fishers’ behaviour included his preferred herbivores, and 14 commercially As part of a larger study of desirability of herbivore species important targets of Micronesian spearfishers (Rhodes across Micronesia, 25 spearfishers were interviewed in et al., 2008) (including the grouper species protected by the March 2009 (Bejarano et al., 2013). Most of these fishers April–July closure) (Table 1). After this, a second scenario resided in Koror and were associated with the spearfishing recreated the grouper closure by removing the photocards catches measured here, whereas others resided in Babeldaob of protected groupers from the set, and fishers were and fished actively (i.e. more than three nights a week) to prompted to rank the remaining species one last time commercialize at least part of their catch. On average, inter- (Table 1). Presenting fishers with both scenarios during viewees stated having been dedicated to fishing for the last open grouper season (March) might have influenced their 29 (±2.9) years. During interviews, each fisher examined 51 responses. Therefore, any potential bias associated with the photocards of locally common herbivores. Cards were pre- timing of the interviews was eliminated by emphasizing to sented to all fishers in small batches containing 6–10 species all fishers that decisions were to be made independently of

Animal Conservation 17 (2014) 133–143 © 2013 The Zoological Society of London 135 Spear ﬁshery of herbivores during closed grouper season S. Bejarano Chavarro, P. J. Mumby and Y. Golbuu the time of year (i.e. assuming that groupers were available Table 2 Species regarded by spearﬁshers as actively targeted, and unavailable as directed, for the purpose of the opportunistically harvested and generally avoided during interviews interview). (n = 25) in Palau Opportunistically Data analysis Actively targeted harvested Avoided Acanthuridae Volumetric and numeric catch per unit effort (hereafter Naso unicornis Acanthurus olivaceus Acanthurus nigrofuscus referred to as CPUEV and CPUEN, respectively) of herbi- Naso lituratus Ctenochaetus striatus Acanthurus nigricans vores were calculated for all landings, using equations (1) Acanthurus Naso tonganus Acanthurus pyroferus and (2): xanthopterus Acanthurus Acanthurus auranticavus = ()()× CPUEV W T F (1) nigricauda Acanthurus maculiceps Acanthurus blochii

CPUEN = () N() T× F (2) Acanthurus lineatus Naso brachycentron where W is the total weight of herbivores within a landing, Acanthurus bariene N is the total number of herbivores within a landing, F is the Scaridae number of fishers contributing to the landing and T is the Chlorurus Scarus festivus Calotomus carolinus total fishing time associated with the landing (including microrhinos Cetoscarus Chlorurus bowersi Scarus quoyi travelling time). Mean herbivore CPUEV and CPUEN were bicolor calculated for each sample period across sampled landings Hipposcarus Scarus prasiognathos Scarus rivulatus (n = 23 and n = 19). Mean CPUE and open season closed season V longiceps CPUE per grouper season were also calculated separately N Scarus Chlorurus bleekeri Scarus schlegeli for species regarded as opportunistically harvested and rubroviolaceus actively targeted by spearfishers in Palau (see Table 2). Scarus ghobban Scarus altipinnis Scarus dimidiatus We used analyses of variance (ANOVAs) to test whether Scarus forsteni Scarus globiceps the grouper closure affected the CPUEV and CPUEN of Chlorurus japanensis Scarus psittacus herbivores and in particular of heavily harvested species (i.e. Chlorurus sordidus Scarus chameleon Naso unicornis, N. lituratus and Hipposcarus longiceps), and Scarus frenatus Scarus spinus species regarded by fishers as opportunistically harvested or Scarus oviceps Scarus niger avoided (Table 2). The overall adequacy of the models was Siganidae tested by examining (1) the plot of residuals versus fitted Siganus lineatus Siganus punctatus Siganus puellus values to look for heteroscedasticity and (2) the normality Siganus argenteus Siganus corallinus Q–Q plot to test for the normality of errors (Crawley, 2007). Siganus canaliculatus Siganus vulpinus To examine if the grouper closure influenced the size Siganus doliatus Siganus spinus composition of the most heavily harvested herbivores, size Siganus punctatissimus frequency histograms were constructed. The skewness (γ1) and kurtosis (γ2) coefficients of the distributions were calculated as measures of their shape, and the significance of both scenario and switched it for a herbivore during the closed coefficients was tested using t-tests to determine if significant season scenario; (2) ranked a herbivore first in both sce- departures from normality occurred (Crawley, 2007). Sig- narios; and (3) ranked a non-protected grouper or a non- nificantly skewed distributions (P < 0.05) reflected a domi- herbivore first in both scenarios. nance of either small- (γ1 > 0) or large-sized classes (γ1 < 0) and significantly leptokurtic distributions reflected a domi- γ > nance of the middle-sized classes ( 2 0), instead of a rela- Assessment of the representativeness of tively even proportion of different-sized classes in the catch. the catch surveys Differences between size distributions observed during open and closed grouper seasons were tested using bootstrapped Long-term data of adequate temporal and taxonomic reso- Kolmogorov–Smirnov tests, such that exact P-values were lutions were unavailable to determine whether the catches calculated performing Monte Carlo simulations (Sekhon, measured here (over 2 weeks) were representative of the 2011). To determine the proportion of immature individuals entire open and closed grouper seasons. However, we in the catches, the size at first maturity (Lm) was obtained obtained the daily sales volumes logged by the manager of using the FishBase life-history tool (Froese & Binholan, the fish market between 2006 and 2011. Data had been 2000) and plotted over the histograms. registered electronically with an elementary level of taxo- To determine if the fishers’ preference for their favourite nomic detail driven by differences in price among items, herbivores changes in response to the availability of and therefore allowed for restricted but informative com- protected groupers, we calculated the percentage of fishers parisons (see Supporting Information Fig. S1). The total who (1) ranked a protected grouper first in the open season daily weight of N. unicornis had been logged separately from

−16 Siganus canaliculatus and assorted reef fish (including marked for N. unicornis (PBKS = 0.2 × 10 ) and moderate −14 parrotfishes, and other rabbitfish and surgeonfish species), for N. lituratus (PBKS = 0.2 × 10 ) and H. longiceps whereas the total daily weight of parrotfishes began to be (PBKS = 0.001). In catches landed during the grouper closure, separated from the assorted reef fish in April 2011. Because smaller sized classes of N. unicornis and N. lituratus predomi-

S. canaliculatus is harvested with barrier nets, catches of this nated over larger ones (PSKEW < 0.001 and 0.001, respec- species fell beyond the scope of this study, and only sales tively; Fig. 4a,c,e). In contrast, N. unicornis of 48–56 cm TL records of N. unicornis allowed for comparisons that were predominated over smaller ones (PKURTOSIS < 0.001; Fig. 4b), informative of the representativeness of our 2009 surveys. and no skewness was evident in the distribution of Catch volumes observed in the market surveys were consid- N. lituratus in the catches surveyed during the open grouper ered significantly different from mean historical sales season (PSKEW = 1). In catches landed during the grouper volumes if they fell beyond the 95% confidence intervals of closure the size distribution of H. longiceps was positively the latter. skewed and significantly leptokurtic (PSKEW < 0.001 and

PKURTOSIS < 0.005), with a peak occurring at 30-cm TL (Fig. 4e). In landings surveyed during the open grouper Results season, size distribution of H. longiceps was also positively skewed (PSKEW = 0.02), but there was no evidence for a = Herbivore landings during open and closed leptokurtic distribution (PKURTOSIS 1). Marked differences in the proportion of immature indi- grouper seasons viduals between grouper seasons occurred only for

Mean herbivore CPUEN was higher during the grouper N. unicornis. Ten times more immature N. unicornis were closure (7.01 ± 1.17 individuals ﬁsher−1 h−1) than in the open caught during the grouper closure (46%) compared to the grouper season (3.94 ± 0.54 individuals ﬁsher−1 h−1) open grouper season (4%) (Fig. 4a,b). In contrast, similar

(PANOVA = 0.02; Fig. 2a). In contrast, mean herbivore proportions of immature H. longiceps and N. lituratus were −1 −1 CPUEV (∼3 kg ﬁsher h ) was unaffected by the grouper caught in both seasons. closure (PANOVA = 0.10; Fig. 2b). Fisher selectivity questionnaires (Bejarano et al., 2013) Naso unicornis, N. lituratus and H. longiceps were the revealed that 10 herbivore species are actively targeted in most heavily harvested herbivores in Palau (Bejarano et al., Palau, whereas 24 are opportunistically harvested and 17 are 2013). Collectively, these species comprised more than 68% of the herbivore catches landed during both open and closed grouper seasons. While the catch volumes (CPUEV) of these heavily harvested species were unaffected by the grouper closure, the mean CPUEN of N. unicornis doubled in the closed grouper season (PANOVA < 0.05; Fig. 3a). The size composition of heavily harvested herbivores in the catch differed between the grouper seasons, and the magnitude of the difference varied across species. Differences in size composition between open and closed grouper seasons were

Figure 3 Mean numeric (CPUEN) and volumetric (CPUEV) catch per

Figure 2 (a) Mean numeric (CPUEN) and (b) volumetric (CPUEV) catch unit effort (±SE) of the most heavily harvested herbivores per unit effort (±SE) of herbivorous fish (i.e. parrotfish, unicornfish, in Palauan spearfisheries during closed (grey) and open (white) surgeonfish and rabbitfish) during closed (grey) and open (white) grouper seasons. (a) Naso unicornis, (b) N. lituratus and (c) grouper seasons. The asterisk indicates a statistically significant Hipposcarus longiceps. The asterisk indicates a statistically signifi- difference. cant difference.

Figure 4 Size distribution of the catch of Naso unicornis (a, b), N. lituratus (c, d) and Hipposcarus longiceps (e, f) during the closed (left) and open

(right) grouper seasons. Skewness (γ1), kurtosis (γ2) and total number of individuals (n) are presented. The asterisks denote that the distribution departed signiﬁcantly from normality (P < 0.01). Shaded regions on the left of each panel indicate the percentage of individuals caught under the size at ﬁrst maturity (dashed line).

generally avoided (Table 2). Collectively, herbivore species The effect of the grouper closure on regarded by ﬁshers as opportunistically harvested and ﬁshers’ behaviour avoided experienced higher CPUEN and CPUEV during the grouper closure than during the open grouper season Although the grouper closure had no detectable effects in

(PANOVA = 0.001 and 0.004, respectively; Fig. 5a). In particu- the CPUEV of some of the most desirable herbivores lar, opportunistically harvested rabbitfishes such as Siganus (Fig. 3), it affected the targeting behaviour in most of punctatus, Si. argenteus and Si. doliatus experienced the the interviewed fishers. Sixty-seven per cent of fishers most obvious increases in CPUEN during the grouper preferred the protected groupers Plectropomus spp. over closure (e.g. 75%; Fig. 5b). The grouper closure coincided their favourite herbivores during open season, but ranked with smaller increases in the CPUEN of the opportunistically their favourite herbivore higher than most other commer- harvested Scarus altipinnis, Sc. forsteni, Sc. festivus and cially important species during the grouper closure. For Acanthurus maculiceps (Fig. 5b). Seven herbivore species 33% of fishers, a herbivore would be their preferred that were not harvested during the open grouper season choice regardless of the grouper season. For 57% of the appeared in the grouper closure catches. Three of these fishers who changed their preferred target during the species were regarded by fishers as generally avoided (i.e. grouper closure, N. unicornis became the first choice and Siganus spinus, Scarus psittacus, Acanthurus blochii, all other herbivores moved up to higher preference A. auranticavus and A. lineatus). rankings.

Figure 5 (a) Mean numeric (CPUEN) and volumetric (CPUEV) catch per unit effort (±SE) of individuals regarded by ﬁshers as opportunistically harvested or avoided, and (b) mean CPUEN per species. Grey and white bars indicate closed and open grouper seasons, respectively.

Discussion did not coincide with the peak reproductive times of the species involved, we discard the influence of seasonal Herbivorous fish are among the main targets of spearfishers spawning on the observed catches. Second, geographic dis- in Palau, and in this short-term study, we quantified changes tribution of the fishing effort may have differed between in their catch levels that may recur yearly associated with the seasons, thus introducing differences in the species compo- seasonal grouper closure. In accordance to our expecta- sition of the catch. Siganus punctatus and Si. doliatus are tions, herbivores were 44% more abundant in the catches forereef inhabitants, whereas Si. argenteus is a cosmopoli- landed in the grouper closure mainly due to the increased tan species widely distributed in both reef areas and catch rates of small-bodied fish. When harvesting groupers seagrasses (Borsa, Lemer & Aurelle, 2007). Higher catches is prohibited, a surplus fishing pressure is allocated to (1) of these species would have been facilitated if fishers fre- herbivore species that are usually caught opportunistically or quented forereef habitats and seagrasses more often in July avoided, and (2) immature individuals of the highly desirable (closed grouper season) compared with March (open N. unicornis. Interviews with spearfishers suggest that a shift grouper season). Although we lack geographic information in their primary targets occurs in response to grouper pro- associated with the surveyed catches to test this hypothesis, tection and may explain, at least partially, the changes both July and March catches contained high numbers of observed in the catch. With changes in the herbivore catches N. unicornis, H. longiceps and Scarus rubroviolaceus species appearing confined to short periods of time a year, it is that are typical of outer reef slopes (Johannes, 1981; Choat difficult to infer definitive negative impacts of grouper & Randall, 1986). It is therefore improbable that the pres- protection on herbivore populations or function. However, ence of undesirable rabbitfish in the catches surveyed we anticipate that potential risks could be highlighted by during the closed grouper season was related to fishing con- locating overlaps between, say, times when species are most centrating in particular locations. Third, it could be argued vulnerable to fishing and periods of increased catch levels or that the appearance of less desirable herbivores during the desirability. grouper closure may be due to indiscriminate fishers par- The grouper closure was associated with increases of up ticipating in the fishing journeys in July and more selective to 75% in the catch rates of opportunistically harvested ones in March. However, catches in the market are usually rabbitfishes, and coincided with more moderate increases landed by three to four groups of regular fishers through- of at least three other undesirable herbivores. Because out the year (S. Bejarano Chavarro, pers. obs.). A further increased fishing pressure on the least desirable rabbitfishes indication of a relaxed selectivity of spearfishers during the may be confined to short periods of time a year (e.g. grouper grouper closure was the presence of undesirable species closure), and these do not coincide with their known spawn- of parrotfishes and surgeonfishes in the catch, including ing times, this is unlikely to represent a problem. Further, those regarded by interviewed fishers as avoided. Although given that the least desirable parrotfishes and surgeonfishes individually neither of the undesirable herbivores would spawn daily (Johannes, 1978a), it is difficult to predict a replace the value of a grouper in the catch, collectively negative outcome emerging from a short-term increase in these may have contributed to maintain the sold weight fishing pressure. Among herbivores, rabbitfishes have life- stable throughout the grouper closure. history parameters that make them relatively resilient to The grouper closure also coincided with an increased fishing (Bejarano et al., 2013). However, with certain species proportion of immature N. unicornis. Potential problems (e.g. Si. doliatus) acting as important Sargassum consumers emerging from a short-term increase in catch rates of imma- across habitats (Fox & Bellwood, 2008), and pairing ture N. unicornis seem plausible. The life-history strategy of rabbitfish species selectively exploiting crevices that are this species confers high vulnerability to fishing (Froese & inaccessible to other reef fish (Fox & Bellwood, 2013), the Binholan, 2000). If this species were overfished, its impor- ecological consequences associated with an intensified tant macroalgal browsing role (Hoey & Bellwood, 2009; fishery cannot be discarded. Rasher, Hoey & Hay, 2013) could be threatened. Potential While it is possible that catches of undesirable herbi- risks of increasing fishing pressure on immature N. unicornis vores were related to spearfishers relaxing their selectivity from a functional perspective may emerge, especially where during the grouper closure to maintain profit, the reason their contribution to macroalgal browsing role was equiva- why this affected mainly rabbitfish is uncertain. A number lent or superior to that of adults. While immature of alternative factors that may explain this pattern must be N. unicornis are unlikely to surpass adults in their browsing explored. First, certain rabbitfish species (e.g. Si. punctatus) impact due to their smaller bite size, small individuals may aggregate on the reef crest to spawn (Johannes, 1978a), be responsible for significant macroalgal removal if/where thus causing short-term localized increases in adult abun- these have high grazing rates and/or are numerically domi- dance. In Palau, rabbitfish spawning occurs generally nant over adults. Anecdotal observations indicate that around the new moon, with a peak spawning season in N. unicornis is already absorbing surplus fishing pressure March–May for Si. argenteus, and October–November for due to the permanent ban of B. muricatum. Increased catch Si. punctatus (Johannes, 1981). By conducting all surveys levels of N. unicornis during the grouper closure demon- on new moon weeks, we controlled for the potential effect strates the possibility of N. unicornis receiving increased of the lunar cycle in rabbitfish abundance. Moreover, as fishing pressure if populations of Plectropomus spp. are increased rabbitfish catch rates in July (grouper closure) severely reduced.

Although preference interviews indicated that herbivores. However, given that subsistence catches were N. unicornis often supplants fishers’ preferred grouper beyond the scope of this study, this hypothesis remained during the closed season, it seems unlikely that this shift in unverified. To the best of our knowledge, no recent estimate targeting behaviour alone could explain the large propor- of the size of the spearfishing population with commercial tion of immature individuals observed during the grouper and subsistence purposes is available in Palau. Therefore, it closure. A more effective way to maximize profit during the is difficult to assess the extent to which the patterns observed grouper closure would be for fishers to focus on large here could be generalized across the country. N. unicornis rather than on immature ones. However, a The herbivore catches are likely to be dynamic in a paucity of large adults in fished areas may have prevented variety of temporal scales and in response to various factors. fishers from doing so. Strong seasonal variations in the Not only are herbivores the providers of a key ecosystem abundance of N. unicornis were observed in the Society function (grazing), but several species are attached to cul- Islands in French Polynesia (Bagnis et al., 1972). Further, tural customs and lore in Micronesia (Johannes, 1981), interviews with fishers and market personnel suggest that hence the importance of understanding the temporal pat- such seasonality also occurs in Palau, with the largest sales terns of their fishery. This study took a first step in under- occurring from December to May. The role of grouper pro- standing the role of the grouper closure in driving temporal tection versus seasonality in driving changes in the size com- variations of the herbivore spear fishery in Palau. A more position of N. unicornis in catches throughout the year comprehensive approach should consider (1) complement- remains to be quantified. An inconvenient synergy between ing the existing information on herbivore spawning aggre- a paucity of adults and an increased probability of being gations and seasonality to include timing and location and targeted may exacerbate the effects of spearfishing on (2) determining if particular life-history characteristics or N. unicornis populations yearly. functional roles enhance the severity of the impacts of the fishery. In particular, describing the spawning rhythms of Si. punctatus and N. unicornis could aid the distinction of fluctuations in the catch levels that are likely driven by Caveats and future research directions increased abundance of adults in fished areas. Given the short temporal scale of our surveys (4 weeks), this Conservation measures aiming to protect commercially study captured a snapshot of the herbivore spear fishery valuable targets are crucial measures for sustainable during both closed and open season for groupers. It is there- fisheries. However, the potential implications of these meas- fore necessary to test whether the catches observed here ures on other taxa must not be overlooked. First, incidental were representative of the catches landed during the entire catch of alternative species may result in these species closed grouper season in 2009, and the rest of the year. becoming popular among buyers, and with time, they may Ideally, we should determine whether the species and size also become habitual targets. Moreover, if increased interest composition observed in July prevailed throughout April– on alternative, yet vulnerable targets (e.g. N. unicornis) coin- June, and if daily catch rates of species harvested cides with (1) spawning aggregations or (2) periods when opportunistically were higher on April–July compared adults are naturally rare, an unfortunate synergy might con- with August–March in 2009. However, catch data with the tribute to overfishing. In the case of Palau, the grouper taxonomic resolution and temporal scale required to closure was associated with relaxed herbivore species selec- conduct such tests were unavailable. In light of the compari- tivity and an increased probability of desirable herbivores sons between historical sale volumes of N. unicornis and being targeted. Although these implications may now catch volumes observed in this study for this species (see appear to be restricted to the closed season for groupers, Supporting Information Fig. S1), it could be argued that similar longer term implications may emerge, if the latter catch volumes of other herbivores may have been misrepre- were overfished. Given that a basic record of herbivore sales sented by our surveys in 2009. However, because it likely volumes is maintained at the studied market in Koror, taxo- responds to wide fluctuations in the abundance of nomic resolution of these records could be improved in the N. unicornis in fished areas, this misrepresentation may not future, with a minimal effort investment. In doing so, a be generalized to all herbivores. According to fishers in valuable and relatively cost-effective tool to monitor herbi- Palau, seasonality of N. unicornis determines the availability vore catches could be developed. Analysis of long-term her- of ‘large and fatty’ individuals, and deposition of fatty bivore sales records would provide useful information to reserves around the gut seems to be a trait restricted to identify responses to conservation measures and design surgeonfish (including Naso), occurring prior to gonad smart fisheries management strategies. development (Montgomery & Galzin, 1993). In addressing the implications of the grouper closure in No illegal offtake of groupers was observed during the herbivorous fishers in Palau, our study measured the grouper season, indicating that the closure is respected at impacts of one of the most common fisheries management least by commercial spearfishers. As enforcement is likely policies (closed reproductive seasons) for a coral reef-based more difficult in the subsistence sector of the spear fishery, multi-species fishery. Our findings may be applicable to the compliance of the grouper prohibition may be compro- other systems where seasonal closures prohibit access mised. Therefore, subsistence catches during the grouper to desirable resources exploited with selective fishing season might be less affected by a relaxed selectivity towards methods.

Acknowledgements Fox, R.J. & Bellwood, D.R. (2008). Remote video bioassays reveal the potential feeding impact of the rabbitfish This work was funded by the National Fish and Wildlife Siganus canaliculatus (f: Siganidae) on an inner-shelf reef Foundation and the Khaled bin Sultan Living Oceans of the Great Barrier Reef. Coral Reefs 27, 605–615. Foundation. The authors wish to thank the staff at the Frisch, A., Baker, R., Hobbs, J.-P.A. & Nankervis, L. Palau International Coral Reef Centre, the Koror State (2008). A quantitative comparison of recreational Department of Conservation and Law Enforcement, Philip Reklai and all the fish market staff in Koror, and three spearfishing and linefishing on the Great Barrier Reef: anonymous reviewers whose comments greatly improved implications for management of multi-sector coral reef the paper. fisheries. Coral Reefs 27, 85–95. Froese, R. & Binholan, C. (2000). Empirical relationships to estimate asymptotic length, length at first maturity and References length at maximum yield per recruit in fishes, with a simple method to evaluate length frequency data. J. Fish Anonymous. (2007). Palau domestic fishing laws 2007. Biol. 56, 758–773. Noumea, New Caledonia: Secretariat of the Pacific Golbuu, Y., Bauman, A., Kuartei, J. & Victor, S. (2005). Community. The state of coral reef ecosystem of Palau. In The state of Bagnis, R., Mazellier, P., Bennet, J. & Christian, E. (1972). coral reef ecosystems of the United States and Pacific Fishes of Polynesia. Papeete, Tahiti: Les Editions du freely associated states: 2005: 488–507. Waddell, J. (Ed.). Pacifique. NOAA Technical Memorandum NOS NCCOS 11, Silver Bavnick, M., De Klerk, L., Van Dijk, D., Rothuizen, J., Spring, MD: NOAA/NCCOS Center for Coastal Moni- Blok, A., Bokhorst, J., Van Haasthrecht, E., toring and Assessment’s Biogeography Team. Van De Loo, T., Quaedvlieg, J. & Scholtens, J. (2008). Graham, T. & Idechong, I. (1998). Reconciling customary Time-zoning for the safe-guarding of capture fisheries: a and constitutional law: managing marine resources in closed season in Tamil Nadu, India. Mar. Policy 32, 369– Palau, Micronesia. Ocean Coast. Manage. 40, 143–164. 378. Hoey, A.S. & Bellwood, D.R. (2008). Cross-shelf variation Beets, J. & Friedlander, A. (1998). Evaluation of a conser- in the role of parrotfishes on the Great Barrier Reef. vation strategy: a spawning aggregation closure for the Coral Reefs 27, 37–47. red hind, Epinephelus guttatus in the U.S. Virgin Islands. Hoey, A.S. & Bellwood, D.R. (2009). Limited functional Environ. Biol. Fish. 55, 91–98. redundancy in a high diversity system: single species Bejarano, S., Golbuu, Y., Sapolu, T. & Mumby, P. (2013). dominates key ecological process on coral reefs. Ecosys- Ecological risk and the exploitation of herbivorous reef tems 12, 1316–1328. fish across Micronesia. Mar. Ecol. Prog. Ser. 482, 197– Jennings, S. & Polunin, N. (1996). Impacts of fishing on 215. tropical reef ecosystems. Ambio 25, 44–49. Borsa, P., Lemer, S. & Aurelle, D. (2007). Patterns of Johannes, R. (1978a). Reproductive strategies of coastal lineage diversification in rabbitfishes. Mol. Phylogenet. marine fishes in the tropics. Environ. Biol. Fish 3, 65–84. Evol. 44, 427–435. Johannes, R. (1978b). Traditional marine conservation Choat, J. & Randall, J. (1986). A review of the parrofishes methods in Oceania and their demise. Annu. Rev. Ecol. (Family Scaridae) of the Great Barrier Reef of Australia Syst. 9, 349–364. with description of a new species. Rec. Aust. Mus. 38, Johannes, R.E. (1981). Words of the lagoon: fishing and 175–228. marine lore in the Palau district of Micronesia. Berkeley Cinner, J., Marnane, M., McClanahan, T. & Almany, G. and Los Angeles, CA: University of California Press. (2006). Periodic closures as adaptive coral reef manage- Johannes, R.E. (1991). Some suggested management initia- ment in the Indo-Pacific. Ecol. Soc. 11, 31–64. tives in Palau’s nearshore fisheries, and the relevance of Crawley, M.J. (2007). The R book. West Sussex, UK: John traditional management. Noumea, New Caledonia: South Wiley & Sons. Pacific Commission. Dalzell, P., Adams, T.J.H. & Polunin, N.V.C. (1996). Johannes, R.E., Squire, L., Graham, T., Sadovy, Y. & Coastal fisheries in the Pacific islands. Oceanogr. Mar. Renguul, H. (1999). Spawning aggregations of groupers Biol. Annu. Rev. 34, 395–531. (Serranidae) in Palau. Marine Conservation Research Fitzpatrick, S.M. & Donaldson, T.J. (2007). Anthropogenic Series Publ.: 144. Brisbane, Australia: The Nature impacts to coral reefs in Palau, Western Micronesia Conservancy. during the Late Holocene. Coral Reefs 26, 915–930. Joseph, K. (2006). Socio-economic impact of the closed Fox, R. & Bellwood, D. (2013). Niche partitioning of season for lobster in Corn Island.RAAS-Nicaragua. Gulf feeding microhabitats produces a unique function for Caribb. Fish. Inst. 57, 87–100. herbivorous rabbitfishes. Coral Reefs 32, 13–23. doi: Kitalong, A. & Dalzell, P. (1994). A preliminary assessment 10.1007/s00338-012-0945-5 of the status of inshore coral reef fish stocks in Palau. In

Inshore fisheries research project: Technical document no. Rhodes, K.L. & Tupper, M.H. (2007). A preliminary 6: 1–21. Kitalong, A. & Dalzel, P. (Ed.). Noumea, New market-based analysis of the Pohnpei, Micronesia, Caledonia: South Pacific Commission. grouper (Serranidae: Epinephelinae) fishery reveals Montgomery, W. & Galzin, R. (1993). Seasonality in unsustainable fishing practices. Coral Reefs 26, 335–344. gonads, fat deposits and condition of tropical Rhodes, K.L., Tupper, M.H. & Wichilmel, C.B. (2008). surgeonfishes (Teleostei: Acanthuridae). Mar. Biol. 115, Characterization and management of the commercial 529–536. sector of the Pohnpei coral reef fishery, Micronesia. Mumby, P., Steneck, R., Edwards, A., Ferrari, R., Gibson, Coral Reefs 27, 443–454. J., Harborne, A. & Coleman, R. (2012). Fishing down a Sekhon, J. (2011). Multivariate and propensity score match- Caribbean food web relaxes trophic cascades. Mar. Ecol. ing software with automated balance optimization: the Prog. Ser. 445, 13–24. matching package for R. J. Stat. Softw. 42, 1–52. Nichols, P. (1991). Republic of Palau: Marine resources pro- files. Honiara. South Pacific Forum Fisheries Agency Report No. 91/59. Supporting information Passley, D., Aiken, K. & Perry, G.A. (2010). Characteriza- Additional Supporting Information may be found in the tion of the Jamaican spearfishing sector. In: Proceedings online version of this article at the publisher’s web-site: of the Gulf and Caribbean Fisheries Institute. (Vol. 62, pp. 235–240). Gulf and Caribbean Fisheries Institute, c/o Figure S1. Bar plots indicating the mean volume of Naso Harbor Branch Oceanographic Institution, Inc. Fort unicornis sold (kg ± 95% confidence intervals) in new moon Pierce FL 34946 United States. weeks of (a) April–July (closed grouper season) versus Rasher, D., Hoey, A. & Hay, M. (2013). Consumer diver- January–March and August–December (open grouper sity interacts with prey defenses to drive ecosystem season) in 2009, and (b) January–December from 2006 to function. Ecology 94, 1347–1358. doi: 10.1890/12- 2010. Asterisks indicate the mean catch volumes observed 0389.1 during our surveys for comparison.