Introduction

Until about a century ago, western culture generally considered the resources of the vast oceans to be inexhaustible. In contrast, some Pacific cultures on small isolated islands have been aware that their resources are limited. Because of the importance of taking reef fishes as a source of protein, Palauans had to know more of some aspects of the biology of reef fishes than is known by science. For example, a Palauan fisher “knew the lunar spawning cycles of several times as many species of fish as had been described in the scientific literature for the entire world” (Johannes 1981).

I was surprised by the similarity of recommendations for coral-reef resource management by a Pacific island culture to that of theoretical fisheries. Yapese culture recognizes that while women directly plant taro and other vegetables and manage livestock in the terrestrial ecosystem, the replenishment of coral-reef resources is variable, not controlled by humans, so the fishermen must manage by controlling themselves (Margie Falanruw, 1998 Yapese Almanac Calendar). The conclusion of a 33-page mathematical analysis of harvesting variable and uncertain resources such as coral-reef fisheries by Robert May of Oxford and his eminent fisheries science colleagues was “What seems really needed is not further mathematical refinement, but rather robustly self-correcting strategies that can operate with only fuzzy knowledge…” (May et al. 1978).

Working with, not against, fisheries

I believe May et al. (1978) did not provide a mechanism for a “robustly self-correcting” system, but “self-correcting” implies negative feedback. In fisheries stocks that are approaching the population carrying capacity, a stabilizing negative feedback occurs because population production is inversely proportional to population stock. In the population growth curve, the inflection point at the center, where the increase in population production is greatest, is where the system switches from positive feedback to negative feedback (Fig. 1). Below this point, positive feedback when stock is reduced can make the system very unstable. As stock is removed by harvesting, the decreased reproductive stock leads to a decrease in population production and this positive feedback can produce depensation or an Allee effect. Harvesting above the inflection increases population production and is working with the system. Harvesting below the point of inflection makes the system very unstable and is working against the system.

Fig. 1
figure 1

A conceptual model of the relationship between the fish stock and population production. As a fisheries stock increases (x-axis), the rate of population production increases (positive feedback between stock size and rate of population production) as long as the stock is below halfway to the carrying capacity. As the stock size increases to over halfway to the carrying capacity, the conditions begin to get crowded and the rate of population production decreases as the stock size increases (negative feedback). Halfway to the carrying capacity is the point of greatest population production which we call the point of inflection because it is the point of change between positive and negative feedback. It is pictured as a cloud rather than a single point because it is constantly changing. Fishery councils often consider overfishing as being at some point less than half of the original unfished population. Roughgarden and Smith (1996) discussed the fundamentally unstable aspects of fishery stocks below the point of inflection and the stability of the system above the point of inflection. Roughgarden and Smith’s marble-bowl metaphor of stability is illustrated

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Roughgarden and Smith analyzed the instability of fisheries management with the positive feedback below the inflection point and found it to be “worse than keeping a marble on top of a dome” (Roughgarden and Smith 1996). They recommended keeping the harvest above the point of inflection to acquire the stabilizing negative feedbacks, thereby “maintaining the stock at this target is like keeping a marble near the base of a bowl (which is possible even on a rolling ship)” (Roughgarden and Smith 1996). In Fig. 1, the point of inflection is illustrated as a cloud, because in the real world, this point is constantly shifting and so neither Pacific islanders nor fisheries scientists can consistently determine its exact location.

In an ideally sustainable system, the amount harvested equals the amount produced. The horizontal line in Fig. 1 indicates the same high value of take on either side of the inflection. Roughgarden and Smith (1996) suggested a more conservative value at 75% of the carrying capacity. Although the high value in Fig. 1 is near maximum production, it may be close enough to the inflection to be at risk of falling into the high-risk zone of positive feedback, or potential collapse. Roughgarden and Smith suggest 75% as a compromise between production and risk.

Since taking a given amount of catch above the point of inflection is more stable and potentially increases population production, while taking the same amount of catch below the point of inflection destabilizes the system, decreases population production and may lead to system collapse, why do many definitions of “overfishing” fall below rather than above the point of inflection? This is likely because most marine fisheries are in regions of the sea that are open to many fishers, so the concerns of fishers focus on taking their rightful amount. This “tragedy of the commons” overrides concerns about increased production or sustainability.

Adjustive management at the village level

The most effective method to promote sustainability is for the government to give authority for making management decisions only to the stakeholders who immediately rely on the resources (Anonymous 2000; Huang et al. 2016). The Constitution of the Republic of Palau begins by stating that each of 16 districts shall have exclusive ownership of all their living and nonliving resources, except highly migratory fish, from the land to 12 nautical miles (22 km) seaward from the traditional baselines. When a village or local community in Palau believes a resource is being overharvested, the village can establish a “bul” (a moratorium), an ad hoc management procedure for modifying fishing rules to fit a specific problem in time and space. The local community can establish a bul. It is not necessary to obtain regulatory change from the central government.

Previously, I used the common term “adaptive management,” but a reviewer admonished me that “adaptive” implies evolution or source of origin. Johannes (1978) proposed that traditional regulatory practices were developed over time by natives as the methods that were most successful in securing a long-term food supply. Foale et al. (2011) documented that the actual origin of the temporary closure of resource availability has often been a result of social or cultural practices. The origins of practices are beyond the scope of this paper, so to make it clear that I am referring to relatively direct and timely ad hoc adjustment of management practices rather than the cultural development of practices, I use the term “adjustive” rather than “adaptive.”

In 1988, a bul was requested on the export of sea cucumbers. Sea cucumbers are a valued food resource on Palau and are usually gathered by women gleaning the reef flats or seagrass meadows. They are also highly valued in Hong Kong where dried flesh of Holothuria scabra and H. lessoni sell for an average price of over $US 300 kg−1 and 13 other holothuroid species each sell for prices averaging over $US 100 kg−1 (Purcell 2014). Sea cucumbers have an unreliable “boom or bust” recruitment, and so a large-scale commercial enterprise in one location is unsustainable. The foreign fishing vessels require large-scale catches because of costs for shipping, maintenance, salaries and other overhead. The only economically feasible procedure is to liquidate the resource and then move to richer sites. In contrast, local residents have an interest in sustainably maintaining the resource. Palauan women found the corporation was removing their ability to take food home, so the women lobbied for a bul on commercial taking of sea cucumbers (Gerald W. Davis, NOAA, pers. comm., 16 Dec 2015).

A bul has traditionally been issued by the village chief. Since foreign enterprise was affecting the resources of several villages, the Government of Palau developed the Marine Protection Act 1994. The act prohibited the commercial export of the more valuable species of sea cucumber. The act also prohibited any export at any time of hawksbill turtles, some fishes (e.g., bumphead parrotfish, Napoleon wrasse) and coconut crab as well as invertebrates taken from the reefs (mangrove crab, spiny lobster, giant clams, sea cucumbers). The act was amended in 2015 to ban all export of any reef organisms, except if they are produced by aquaculture (e.g., giant clams, corals). Even some cultured species such as coconut crab and mangrove crab cannot be exported, but may be sold only in local restaurants and markets. It may be the case that the populations of coconut crabs in the wild do not grow fast enough to supply the local human population, let alone the international market. Females reach sexual maturity in 9 yr in the wild (Sato et al. 2013).

The act also originally banned the harvest of reef fishes between 1 April and 31 October, the main spawning season of the important reef food-fish species. Palauan fishers requested this regulatory act from the Palauan government to protect against their perceived loss of grouper spawning aggregations (Johannes 1998). Rather than require extensive studies to determine the exact point of overfishing, their adjustive management is based on knowledge of natural history such as time of spawning and locations of aggregations which made them vulnerable (Johannes 1998). In contrast, the developed countries have greatly influenced the economic guidelines of Caribbean cultures. The Nassau grouper was one of the most important food fishes that provided protein for many coastal villages in the Caribbean for many decades, but it gathered in aggregations up to tens of thousands which made it easy to harvest on a large scale. As a result, 60% of the spawning aggregations were eliminated (Sadovy de Mitcheson et al. 2008). There were a number of studies done during the severe decline. Protection has eventually been developed for some of the Nassau grouper spawning aggregations in the Caribbean, but the adjustive management of the Palauan bul (moratorium) was more effective in biological time.

Biological time and space

Some Pacific islanders practice adjustive management by modifying regulations in a biologically meaningful timescale, while first-world countries often act on a timescale based on legal process and politics. For example, the citizens of American Samoa perceived that their large parrotfishes were becoming unavailable to them because they were being overfished by commercial spearfishers operating at night with scuba. Public hearings were called, and upon hearing testimonies of dozens of citizens, the governor issued an immediate executive order to ban spearfishing with scuba at night until the issue was resolved. The commercial operation then moved to Independent Samoa where nine villages rapidly issued a moratorium on spearfishing with scuba and petitioned the government to make their ban national.

In contrast, the establishment of areas for marine reserves on Guam took 15 yr as a result of Guam’s westernized legal and political processes, during which time the yearly nearshore catch steadily decreased 78% from 90 to 20 metric tonnes (data from Division of Aquatic and Wildlife Resources, Government of Guam). Tafileichig and Inoue (2001) concluded that traditional resource management in Yap is more efficient and proactive than the western legislative system of governance. It is a fundamental issue that we should frame our economic and legislative processes to the timescale of biological processes, rather than assume that biological processes can be adjusted to our legislative protocol. The precautionary principle is consistent with the ability of local adjustive management to declare a moratorium until the issue is examined and determined, in contrast to western legal or political frameworks which require the issue be studied and resolved before action is taken.

The scale of space should be accommodated as well as time. On some island groups such as the Hawaiian Archipelago and Palau, indigenous residents act as if they perceive the functioning of their ecosystem from the tops of the mountains to the sea, with property boundaries based on watersheds (e.g., “ahupua’a” in Hawaiian tradition), so that upslope and downslope aspects of the system are typically managed within the extended family or village. Minister Umiich Sengebau is presently mobilizing the action of villages in managing their freshwater and soil resources through their Belau Watershed Alliance. Kitalong (2012) details the cooperation among women of a village in managing the dynamic irrigation adjustments for taro patches and is now accommodating sea-level rise. In contrast, property lines on continents are often defined legally, without consideration of ecosystem processes.

Export from coral reefs is not natural

In October 2015, Palau became the first nation to fully protect by 2020 more than 80% of its exclusive economic zone (EEZ) from any fishing, with about 20% remaining open only to domestic fishers who may sell their catch to local restaurants, hotels and markets (Fig. 2). Foreign fishers will not be allowed to operate within 200 miles (322 km) of any of the islands of Palau. To pay for the maintenance of a protected areas network (PAN) and for the loss of fishery revenues from the EEZ, the Palau Government established a Green Fee, an exit tax that is paid by anyone traveling out of Palau. The tax revenues to Palau from scuba-diving tourism were 24 times higher than the total revenues from the fishing industry (Vianna et al. 2010). The United Nations awarded Tommy Remengesau Jr., President of Palau, a Champion of the Earth award for policies that sustain economic success while maintaining natural resources.

Fig. 2
figure 2

A map of the entire exclusive economic zone of Palau (approximately 600,000 km2 area within the solid line) which will not be available to foreign fishing activity by 2020. Local fishermen are allowed to fish for open-ocean fishes in 20% of the EEZ (cross-hatched region around the main islands of Palau). Individual districts have exclusive jurisdiction over the resources on their reefs and coastal waters from shore to 22 km out to sea (light areas within the dashed lines)

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Local consumption rather than exportation is the natural process of the coral-reef ecosystem. Coral-reef ecosystems naturally export only about 1% of their gross primary productivity. Nixon (1982) determined that coral reefs generally had a very high gross primary productivity, about ten times that of other marine ecosystems per unit area, but relatively little excess productivity or potential fisheries yield (about a tenth of upwelling marine systems). Therefore, the ratio per unit area of net community or excess yield to gross primary production in coral-reef systems is about 1% that of systems with high fisheries yield. Hatcher (1997) found an upper limit of sustainable export from the coral reef to be about 2–3% of gross primary productivity, but of this, only about 10% is useful to humans (fisheries yield). The rest is mucus, dissolved organics and detritus. So the ratio of useful excess to gross productivity by this approach is also <1%. Kinsey (1983) reviewed the literature on the metabolic performance of undisturbed coral reefs from around the world and found the ratio of gross diel respiration to gross diel primary productivity was usually close to one (1 ± 0.1), which corroborates the disparate approaches of Nixon and Hatcher.

The reason there is so little export from natural, undisturbed coral reefs is probably because the production is consumed by the diverse array of animals and microbes across several trophic levels (Birkeland 2015). Atkinson and Grigg (1984) estimated the net benthic primary production at French Frigate Shoals in the Northwest Hawaiian Islands as 4.1 × 106 kg km–2 yr–1, while Polovina (1984) calculated the net benthic (algal and coral zooxanthellae) primary production necessary at the same site to support the ecosystem to be 4.3 × 106 kg km–2 yr–1. Primary production of phytoplankton explains only 3% additional primary production (Polovina 1984). If 5% more is consumed than is produced, this might be explained by input to coral-reef communities of materials sourced from outside the ecosystem, e.g., by oceanic zooplankton, open-ocean fodder fishes contacting reefs, or by reef fishes going out and foraging in neighboring habitats such as seagrass meadows (Ogden et al. 2014). The conclusion is, if more is consumed than is produced on site, this is consistent with the concept that little may be naturally exported because much of the production is consumed within the system.

Economists consider the export of long-lived, or irregularly recruiting, coral-reef species as a “gold rush,” i.e., depleting the local resource and moving on (Anonymous 2000). This is because the expense of operating ships and personnel when commercially harvesting, transporting and marketing of the live-reef-fish trade, giant clams, sea cucumbers, coconut crabs, etc., requires extraction beyond the level of production. The coral-reef resource needs to be liquidated in order to gain a profit above the expense of operation. Additionally, species such as sea turtles that take a couple of decades to reach maturity, or species such as sea cucumbers that reproduce irregularly on a harvestable scale, depreciate if not liquidated. The money from liquidation can grow faster by investment or interest than the resource can increase by growth and reproduction, so liquidation is the best procedure economically.

The goal of developed countries with wide-ranging ships is to increase the proportion of excess production, and this can be accomplished by reducing the biomass in the upper trophic levels. If the upper trophic levels and large individuals are reduced, then the net production that they would have consumed can be sidetracked to excess production. We essentially remove our competitors. This has been widely achieved in the world’s fisheries (Pauly et al. 1998; Fenner 2014). Additionally, there is often more rapid growth and population turnover in lower trophic levels and smaller individuals (DeMartini et al. 2008).

In coral-reef ecosystems, reducing the biomass at upper trophic levels and removing the fishes of larger body size work against the stability of the system because large fishes are exponentially more fecund than are medium-sized fishes, some species are sequential hermaphrodites, and the larger herbivorous fishes are qualitatively and quantitatively more effective in engineering habitat by influencing benthic community dynamics (DeMartini and Smith 2015). Analyses of data from 251 populations of fishes found that as recruitment success became more variable or unreliable, the traits of late maturity, increased longevity and iteroparity increased (Longhurst 2002). The larger fishes at upper trophic levels on coral reefs are generally characterized by these traits, which suggests that successful annual recruitment is unreliable and their populations are not likely to maintain stock reproductive potential if most of the large individuals are removed. Retaining a substantial stock of large individuals is working with sustainable yield in the long term.

There is an adage that there should be a minimum size limit in the taking of fish to allow at least a first reproduction. This does not work for many, perhaps most, species of reef fishes because they rapidly grow to maturity and then stay at approximately that size for decades (Choat and Robertson 2002). For example, Naso unicornis in Hawaii reaches adult size in 2–3 yr and then lives at that approximate size for over 50 yr (Andrews et al. 2016). This indicates that reproduction from 1 or 2 yr of adulthood cannot guarantee recruitment success and the species has evolved the capability of multiple years of repeated attempts (Longhurst 2002). The population of such species must be allowed the continuation of a substantial portion of the mature individuals in the reproductive stock, not just those that have reproduced once or twice.

The average subsistence reef-fishery catch in Palau over 20 yr from 1985 to 2005 had been 1200 t yr−1 (Golbuu et al. 2005). This may have since stayed fairly stable considering Gillett (2016) calculated the coastal subsistence catch in 2014 to be about 1250 t. Palau has 525 km2 of reef (Yukihira et al. 2007), so the subsistence fishery yield of Palauan reefs is approximately 2.3 t km−2 yr−1. Although the sustainable yield of coral-reef fisheries in other regions may be sometimes as high as 5 t km−2 yr−1 (Newton et al. 2007), the fishers of Palau over the past decades have gradually been having to go farther and stay longer to harvest enough seafood (Kitalong 2012). This may be partly because there is also some commercial fishing as well as subsistence fishing, but commercial reef fishing has on average harvested only about 1.1 t km−2 yr−1 during the 20 yr between 1985 and 2005 (Golbuu et al. 2005). It may be that this has been mostly because of a reduction in replenishment success resulting from differential removal of larger-bodied fishes, rather than a reduction in biomass.

Biomass can be a metric for changes in fish stock over time or for comparisons between stocks, but it is not informative for the condition of the population. Houk and colleagues monitored 21 sites across four islands in the Northern Marianas for 12 yr before, during and after disturbance events. They found the fish biomass before the disturbance had no predictive value for recovery, but fish size before the disturbance was a consistently good predictor of resilience (Houk et al. 2014). Hsieh et al. (2006) found that fishery-induced truncation of age structure substantially increased variability in recruitment to populations before the fishery measurably affected population abundances. McClanahan (2014) at five sites from 0.4 to 28 km2 in southeast Kenya and McClanahan and Graham (2015), analyzing fish survey data from 324 sites across eight countries at the Indian Ocean, showed that fish biomass recovered in less than half the time it took for functional ecology and life-history characteristics to recover. Restoring biomass alone is insufficient to bring the system back functionally. Depleted stocks should not be open to renewed fishing when the biomass is back to the original level, but need to have their historical age distributions restored before fishing is resumed (Anderson et al. 2008).

Palau may have recently started the recovery of potential fisheries production with the Protected Areas Network Act 2003 and the Micronesia Challenge of 2006, establishing at least 30% of the nearshore area of Palau as protected for enhanced replenishment of fisheries stock. After a decade, permanent protected areas now have larger fishes, two to three and a half times the fish biomass, and five times greater biomass of top predators than the control (unprotected) neighboring areas (Friedlander et al. 2014). Fish populations can be substantially fished down in a few weeks (Jupiter et al. 2012), but in a long-term study in the Philippines, Russ and Alcala (1996) found that the recovery of larger reef fishes did not begin to occur until at least the fifth year of protection. It took decades (20–40 yr) for the larger predatory fishes to regain their initial size distributions (Russ and Alcala 2010; Abesamis et al. 2014; McClanahan 2014). Using census data from 324 coral reefs in the Indian Ocean, McClanahan and Graham (2015) found that biomass may recover in about 20 yr, but to recover the original size distribution may take over 100 yr.

Because of the ability of fishers to rapidly reduce stock substantially (within weeks or months) and because of the slowness of rebuilding stocks to their natural state (decades), rotational or periodic closures are sometimes not effective (Cohen and Foale 2011, 2013; Goetze et al. 2016). The monitoring of periodic 1- or 2-yr closures 1978–2002 near Honolulu, Hawaii, provided a demonstration that over 25 yr, the total biomass declined about 67%, the biomass of targeted fishes declined about 75%, large fishes were nearly absent, and there was no meaningful recovery of ecological function. The yield (0.6 t km−2 yr−1 in the periodic opening) and catch per unit effort (CPUE) were generally better in perpetually open areas (Williams et al. 2006). Part of the reason for the better performance of perpetually open areas is that there was especially intense fishing pressure with each opening of the periodic closure. For example, in 2000, 82 spearfishers entered the water at 0800 hrs on the opening day of the rotational closure near Honolulu that had been closed for 1 yr (Meyer 2003). Cohen and Foale (2013) documented similar patterns of decrease in long-lived stock over time in periodic closures in the South Pacific. They concluded that it was essential that the fish taken during openings should not exceed the replenishment that occurs during closure. Considering the decades it takes for large predatory reef fish to recover, periodic closures may not be practical.

Slot-limit fishing (here defined as allowing the harvest of intermediate-sized fish, while protecting smaller fish until after first reproduction and the larger fish that are near their asymptotic length) may have more potential for food security when harvesting coral-reef fishes than most periodic closures. Fecundity increases exponentially with body length in fishes, and so one could harvest several times the biomass of medium-sized individuals rather than large ones, yet have substantially less effect on the reproductive stock potential. Further, a well-managed harvest could be continuous by slot-limit, rather than periodic. In the section later in this paper on west Hawaii, it is suggested that slot-limit fishing and predation may facilitate the sustained yield of hundreds of thousands of fish per year from a part of the west coast of the island.

Focus harvesting on open-ocean, not reef, fishes

The 2.3 t km−2 yr−1 subsistence fishery yield provides the resident population of Palau (21,311 on 7 July 2016, UN Dept Economic and Social Affairs: Population Division) with an average of 56 kg of fish individual−1 yr−1. However, the number of visitors to Palau (167,966 in 2015, Office of Planning and Statistics, Government of Palau) is nearly eight times as many. Visitors stay only 6 d on average, so the visitors on any single day may increase the number of humans by only 12.5%. Nevertheless, although Palau bans the export of resources, fish are being surreptitiously exported in the stomachs of 167,966 visitors.

Palauans can probably sustain a subsistence reef fishery for themselves, especially if they leave a substantial portion of the large individuals in the targeted species, but tourists should be fed mainly open-sea and other non-reef fishes with more r-selected life histories. Unlike coral-reef fishes, most open-sea and other pelagic fishes have rapid production and turnover (Fig. 3). Fishes such as yellowfin tuna, mahi-mahi and skipjack grow remarkably fast. Yellowfin can reach 15 kg in one year, 30 kg by year two and 70 kg by seven years. Mahi-mahi can reach 16 kg in only 8 months and 35 kg at four years (Pepperell 2010). These species rarely live ten years. Coral-reef fishes generally do not grow to these sizes, and those that do grow much more slowly (Fig. 3). Many targeted species of reef fishes live for decades (Choat and Robertson 2002; Andrews et al. 2016), and so production and turnover are very much slower on coral reefs than in the open ocean. Modern technology may soon encourage opening the vast new resources of the deep-reef slope, but available evidence indicates that deep-reef fishes also typically grow much slower and live much longer than open-ocean epipelagic fishes (Andrews et al. 2011, 2012).

Fig. 3
figure 3

A comparison of the rates of growth and longevities of typically targeted open-ocean and coral-reef fishes. Targeted open-ocean fishes grow relatively rapidly and are relatively short-lived compared to targeted coral-reef fishes. The y-axis indicates the approximate maximum size of individuals of a species or genus at the age indicated on the x-axis. The open-ocean fishes are yellowfin tuna (YF), mahi-mahi (MM), skipjack (SJ) and bluefin tuna (BF) (Pepperell 2010; www.fishbase.org). The coral-reef fishes are Acanthurus spp. (Ac), Naso unicornis (Nu), Epinephelus fuscoguttatus (Ef), Lutjanus spp. (Lj), Epinephelus striatus (Es) and Bolbometopon muricatum (Bm). The vertical marks for the genera of Acanthurus and Lutjanus indicate the life spans of the species with the shortest, average and maximum known longevities (Choat and Robertson 2002; Andrews et al. 2016; www.fishbase.org)

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Not only is the potential excess yield per km2 about ten times greater in the open ocean because of fewer trophic levels (Nixon 1982; Birkeland 2015), the oceanic area under the jurisdiction of Palau (about 600,000 km2) is over 1140 times the area of coral reefs (525 km2; Yukihira et al. 2007). This greater area of the open ocean is especially effective because open-ocean fishes roam throughout, rapidly replacing harvested stock, while coral-reef fishes are relatively residential so replenishment of a harvested stock needs the slow and complex process of local recruitment. Fundamentally different ecosystem processes between the open ocean and the coral reef makes the pelagic fisheries less sensitive to harvest. The productivity of the open ocean is greatly influenced by the upwelling of nutrients, but overharvesting blue-water fish does not influence these oceanographic processes. In contrast, the overharvesting of reef fishes, especially herbivores, can change the characteristics of the ecosystem (Rasher et al. 2013; DeMartini and Smith 2015).

In Hawaii, reef fish (68%) and bottomfish (38%) dominated restaurant menus from 1928 to 1940, but after World War II, the tourist industry grew and demand for food supply increased exponentially. Coral reef and bottomfish drastically declined by 1960 and now nearly all menus are dominated by open-ocean fishes (Van Houtan et al. 2013). Perhaps this same transition could come with the increase in tourism in Palau. Japanese and westerners should have no trouble being served open-ocean fishes in Palau, but the Chinese and Taiwanese appear to have a propensity for choosing reef fishes. Much of the live-reef-fish trade is to Hong Kong, China and Taiwan where restaurants still serve coral-reef fishes (Huang et al. 2016). This may be a problem for Palau where 61% of the visitors in 2015 were from China and Taiwan.

Shift away from coral reefs to higher yields with nearshore pelagics

The relatively slow-growing, late maturing, targeted coral-reef species, with site fidelity and decades of multiple attempts required to reproduce successfully on reefs, will not be able to sustain the populations of fishers as islander populations grow. If islanders do not have the financial resources to start open-ocean fishing, they may need to develop methods to harvest nearshore pelagics. Smaller nearshore pelagics (such as scads, mackerels, small schooling barracudas, and clupeids like herrings, anchovies, and sardines) are fast-growing, early reproducing, short-lived, wide-ranging fishes that occur in large schools and that can potentially sustain relatively heavy fishing for decades. Smaller pelagic nearshore carangids (scads), Selar crumenophthalmus (akule) and Decapterus macarellus (opelu), have provided such large catches each year in Hawaii that the commercial and recreational fishing groups, a native rights group, and state and national agencies all expressed concern that the nearshore pelagics were likely being overfished. However, the short time to maturity (7 months for akule, 18 months for opelu) and rapid growth (asymptotic length occurs at 1–2 yr and at 2–3 yr in akule and opelu, respectively) indicate that they have not been threatened by fisheries over a period of three decades (1966–1997) of harvest (Weng and Sibert 1997). W.J. Walsh (unpublished data, Division of Aquatic Resources, State of Hawaii) examined 64 yr (1949–2013) of catch records of opelu in a relatively heavily fished section on the southwest coast of the island of Hawaii. Over the decades, there was a general decrease in catch per fisher, but over recent years the catches have been fairly stable and substantive. Likewise, in the Philippines, Porfirio Aliño reported a substantial decrease in CPUE between 1948 and 2000, yet the total annual catch of small pelagic fish stayed relatively constant (www.innri.unuftp.is/pdf/Philippine%20Fisheries.pdf). The catch of akule between 2003 and 2012 was 103,971–114,854 t and the catch of Decapterus (the genus of opelu) was 310,639–233,482 t (www.fao.org/fishery/facp/PHL/en and www.fao.org/fi/oldsite/FCP/en/phl/profile.htm). Therefore, even if overfished, nearshore pelagics have the potential to sustain some fishery for much longer than is likely for coral-reef fishes and, unlike coral-reef fisheries, nearshore pelagics are likely to recover in less than decades if allowed to do so by implementing local precautionary management.

Furthermore, the CPUE of nearshore pelagics can be potentially larger than coral-reef fisheries because of the possibility of using light and/or platforms to aggregate fish from a relatively wide area for bulk harvest. Nearshore pelagics tend to range over an area in larger numbers in a shorter amount of time than reef fishes. In a plankton-based trophic system, the zooplankton can be attracted by light into a concentration which can attract and aggregate the smaller nearshore pelagics, which in turn can attract the larger predatory pelagics. Bagans are large floating catamaran platforms with a light to attract the zooplankton and fish. There is a large net below the bagan that can be raised to take most of the fish aggregating beneath the light. On a smaller scale, individual or pairs of fishers in dugout canoes can attract nearshore fish by light and scoop them up with a hand net (Roeger et al. 2016).

Bagans in Indonesia and the Philippines also can attract whale sharks. The local villages sometimes gain a supplemental income by charging a fee from tourists for diving with the whale sharks. For live-aboard dive ships, each of the crew can be charged as well as the tourists, even though they do not all observe the whale sharks. In the Philippines, fishers in dugout canoes that attract whale sharks are sometimes paid individually by the tourists.

Platforms with dangling materials (fish aggregating devices, FADs) that attract smaller fish, which in turn attract larger fish, can also concentrate resources, even without lights. FADs are disapproved by many conservationists and non-governmental organizations (NGOs) and are occasionally called floating atoll destroyers. This is because they can damage coral reefs and can also lead to overharvesting of pelagic fishes. However, governments or NGOs working to improve food security for local villages and CPUE for local fishers should consider FADs, but with improved design. FADs or bagans should be at least a kilometer away from coral reefs, but within accessible range of the kinds of boats used by the village (Bell et al. 2015). The use of local FADs should be limited to local residents and not available to outsiders, especially from other nations. Local FADs should not be equipped with signaling devices that may attract large fishing boats. FADs should be anchored very securely to prevent them washing up on coral reefs and dragging across corals, possibly introducing alien species if originating from very far away. Dangling materials should be flat wall structures, not nets or ropes to prevent sea turtles, sharks and other organisms from getting entangled and dying. Although FADs may have the potential to facilitate the overharvest of resources, the life-history traits and demography of nearshore pelagics make them potentially more resilient to harvest than are coral-reef fishes.

A caveat to attracting wide-ranging fishes such as nearshore pelagics with lights or with shelter beneath a platform is that the fish are potentially being harvested in bulk from a large area. They could be so effectively attracted from a large area that they may continue to supply a good catch even while the population is in substantial decline. Furthermore, the bulk catch in the net includes both immature and reproductive stock. The fishers might be unaware of the decline and this could be a serious matter if there were a large number of bagans in the area. Nevertheless, although it is possible to overharvest nearshore pelagics, their rapid growth, early and frequent reproduction and their movements in large shoals potentially make them more resilient to frequent harvest than most coral-reef fish species.

The increased input of nutrients into coastal waters of high islands from terrestrial runoff and river discharge has become widespread. This especially affects partially enclosed bays and lagoons (Caddy 2000). Although excess nutrients can affect benthic autotrophic systems negatively, trophic systems based on phytoplankton can be enhanced by nutrient enrichment. The potential production of nearshore pelagic systems may be increased in the future, while the production of shallow tropical benthic systems may decrease (Gehrke 2007). Of course, where nutrient runoff or river discharge carries enough agricultural fertilizer to cause hypoxia, all affected systems are degraded.

Palau leads other nations

Traditional island cultures in Polynesia and Micronesia sometimes have similar traits that are supportive of sustainability such as reef tenure, but the present success or status of these cultures varies widely as a result of differential effects of foreign cultures in the twentieth century. Across Oceania, the daily activities of traditional cultures were greatly affected by the settlement from developed countries that brought money-based social organization, advanced technologies, export markets and a replacement of the traditional subsistence social economy with profit motivation. Palau did not experience a favorable history of events. In 1940, Palau was home to a commercial society of 23,000 Japanese and only 7000 Palauans. The Palauans had to severely overharvest their resources during World War II to feed Japanese soldiers that were cut off from supply lines.

The recent policies established for resource management are directly the result of the leadership of individual Palauans such as Noah Idechong, President Tommy Remengesau, Jr., Minister Umiich Sengebau and scientists Yimnang Golbuu and Steven Victor, not the result of a grassroots movement based on the culture and knowledge of Palauans. However, I believe the Palauan leaders were successful in their policies in part because they were skilled communicators and in part because both the new policies they were promoting and the traditional cultures were congruent with the biology of their resources.

Noah Idechong, a fisherman from Palau with a college degree in business administration from Hawaii Pacific University, became the founding director of the Palau Conservation Society (PCS), a NGO with the goal of strengthening proper management of marine and terrestrial resources by local communities. Working with both local communities and with the national government, PCS developed the PAN. Palau also took the lead on the creation of the Micronesia Challenge in which nations of Micronesia all pledge to conserve effectively at least 30% of their nearshore marine resources and 20% of their terrestrial resources by 2020. PAN sites will be the Palauan fulfillment of its promise to the Micronesia Challenge.

In 2006, Palau began a ban on any fishing for sharks throughout its 600,000 km2 EEZ. This was followed in 2010–2015, by the Maldives, the rest of Micronesia (the Marshalls, Kosrae, Pohnpei, Chuuk, Yap, the Commonwealth of the Northern Marianas, and Guam), Tokelau, Raja Ampat, Honduras, the Bahamas, American Samoa, French Polynesia, the Cook Islands, the British Virgin Islands, Bonaire and Saba, banning the taking of sharks anywhere in their respective EEZs. In 2016, the Galápagos established the northern section of its EEZ as a shark haven. These 20 EEZs provide a total of 12,046,891 km2 of no-take shark reserves, including both nearshore and pelagic habitats.

What if other nations followed Palau’s lead in not allowing foreign fishers to operate within 200 miles (322 km) of any of their islands, closing their entire EEZs to foreign fishers? This would protect their natural resources while they could build and globalize their economies though service-based industries.

West Hawaii ornamental fisheries

Village-level control of fisheries backed with government support can succeed in the USA as it has in Palau. The West Hawaii Fishery Council (WHFC) is composed of a broad array of stakeholders in the local community (including commercial, aquarium, recreational and subsistence fishers, tourism operators, conservationists, businessmen and citizens). Under the guidance of local leaders such as Bill Walsh and chairs of the WHFC, the total annual catch of ornamental fishes in west Hawaii increased nearly eightfold in the past 30 yr, and the total economic value of the catch increased nearly fourfold (Walsh 2014). The take by the aquarium industry of Zebrasoma flavescens (yellow tang) along the west coast of Hawaii has exceeded 300,000 individuals yr−1 for a decade. This has certainly been in part because the WHFC has set aside about 35% of the coast as reserves, but it is possibly also because larger individuals are left for population replenishment. In addition, the introduced predator Cephalopholis argus cannot efficiently prey on larger individuals (Meyer and Dierking 2011). Slot-limit fishing and predation may both be occurring and contributing to a sustainable fishery.

Legislative protocol or biology?

The performance of the WHFC indicates that local resource management can work in modern developed nations as well as in remote islands. Our acceptance of this is resisted by our fundamentally different cultural heritage. Although technically developed first-world societies no longer champion the sea as inexhaustible, many management practices originally developed under this paradigm continue. A major problem is that the resources of the sea legally belong to everyone; therefore, it is assumed they can be taken by anyone. This is deeply rooted in politics, law and economics and is the primary driver of competition and overcapitalization in the “race to fish.” One approach taken by first-world countries to resolve this problem is to give the authority to make management decisions to the fewer stakeholders that immediately rely on common resources through allocation by bidding on individual transferable quotas (Little et al. 2011). On land, humans have had a history of being closer to resources and so biology is still recognized. Songbirds and wild game belong to everyone, but people understand that the biology of the system will not encourage the harvest and export of song birds and wild game for food. The leaders of Palau know that the biology of reef fish and coral-reef ecosystems does not allow exportation for food.

A common assumption is that we can no longer think in terms of biology because the local human population is now too large and densely concentrated in places like Honolulu and Miami. Overharvesting of reef fish is often considered inevitable near large human population centers. But people in Honolulu and Miami do not take their beef, pork and chicken locally. They are imported from well-managed farms. Likewise, their fish should be imported from a well-managed open sea, not the reef, supplemented by aquaculture. It is imperative that we frame our economic and legislative processes to the scale of time and space of biological processes, rather than assume that biological processes can be adjusted to our legislative protocol.