Background

Tag technologies

Historically, insights into the behavior and ecology of large pelagic fishes in their natural environment were limited to those obtained visually and at the ocean’s surface. These constraints allow access to only a small portion of a species’ behavior, and it has long been recognized that novel approaches are needed to better understand pelagic fishes. Mark-recapture techniques employing external tags have been used extensively since the early twentieth century, but this approach only provides deployment and retrieval locations with no data on a fish’s behavior in the interim [1].

The development of electronic tags enabled researchers to gather a more holistic view of the behaviors of large pelagic organisms. By the 1960s, acoustic technologies were used to actively follow a single-tagged individual for short periods (up to 2 weeks). Longer term datasets became available in the early 1980s with the development of passive acoustic techniques that were well suited to long-term monitoring of high activity regions such as seasonal aggregation sites [2].

Satellite-linked archival tags are the latest development in telemetry research and have demonstrated considerable promise. Since their inception, these tags have been increasingly deployed to understand horizontal and vertical movements [3-6], residency [7], mortality [8], aggregative and feeding behaviors [9], and other important aspects of the biology and ecology of marine organisms. This technology, coupled with large-scale deployment efforts that focus on different species and geographical regions, facilitates extensive data collection. These datasets are amenable to insightful literature reviews and syntheses that can provide valuable information on biophysical drivers and species ecology. While such a review has been performed for sharks [10], a synthesis of the biophysical interactions evident from the numerous satellite tagging studies on billfishes has not yet been undertaken.

Stock status

Herein, we use “billfishes” to apply to the Istiophoridae and the Xiphiidae, two families of large, predatory fishes that inhabit the pelagic realm [11]. Billfishes (suborder Xiphioidei) are distinct from the scombroids [12] and comprise the sailfish and marlins (family Istiophoridae) and swordfish (of the monotypic family Xiphiidae). Ten billfish species have been identified [12]. Three species occur worldwide while three are restricted to the Atlantic, three to the Indo-Pacific, and one to the Mediterranean (Table 1).

Table 1 Billfish taxonomy and pop-up satellite tagging effort to-date
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Swordfish and several tuna species are major targets of large- and small-scale, directed commercial fisheries around the world. Istiophorids are largely targeted by lucrative directed recreational fisheries, but bycatch from tuna and swordfish pelagic longline (PLL) fisheries is the source of most fishing-induced mortality. Artisanal handline fisheries also yield significant pressure on some species [13]. These compound to result in overfishing of many billfish stocks [14], but stock status varies among and within species and ocean basins.

Historically, commercially valuable fishes, like swordfish, have been overexploited. Yet, despite their economic value, swordfish now appear to be adequately managed throughout the Atlantic and Pacific [15], with North Atlantic stocks exhibiting recovery after years of overfishing[16,17]. However, Mediterranean swordfish stocks are currently both overfished and data deficient [18].

Assessments of blue (Makaira nigricans) and white marlin (Kajikia albida) by the International Commission for the Conservation of Atlantic Tunas (ICCAT) indicate a significant decrease in landings of both species since the 1950s [19]. Catch data and modeling efforts indicate that both populations are below biomass levels for maximum sustainable yield (MSY) and are poorly managed despite robust ICCAT management criteria [20]. Blue marlin have historically been heavily overexploited, largely as bycatch from the PLL fleet [21], and have demonstrated up to a 64% population decline over three generations [15]. Pacific populations of blue marlin are also poorly managed and likely declining [15]. White marlin biomass reached historic lows at the turn of the twenty-first century [22] and was estimated at 15% of maximum sustainable yield (MSY) [23]. This has fostered multiple, though unsuccessful, attempts to list white marlin as threatened or endangered under the U.S. Endangered Species Act.

Sailfish (Istiophorus platypterus) are currently managed as two separate (east and west) stocks in the Atlantic, and both are considered overharvested [24]. Pacific populations are also declining but assessments are data deficient [15]. Due to similar data deficiencies, both black (Istiompax indica) and striped marlin (Kajikia audax) are lacking full stock assessments. Both species are caught as bycatch in other fisheries and are likely declining; striped marlin have declined by >20% globally in three generations [15].

Little biological, ecological, or population-status information is available for the spearfishes: shortbill spearfish (Tetrapturus angustirostris), longbill spearfish (Tetrapturus pfluegeri), roundscale spearfish (Tetrapturus georgii), and Mediterranean spearfish (Tetrapturus belone). Shortbill spearfish are often included in aggregate catch statistics and are thus considered data deficient. Longbill spearfish are not a target of any large-scale fisheries, whereas roundscale spearfish are almost completely unstudied [25]. Mediterranean spearfish are in decline as both a target (e.g. Strait of Messina) [26,27] and non-target species (Aegean Sea swordfish driftnet fishery) [28]. Given that the data-deficient spearfishes are often caught on the same gear as targeted species, they may be experiencing similar declines [29].

One particularly confounding effect of our understanding of white marlin and roundscale spearfish populations in the Atlantic is the recent evidence that some roundscale spearfish have long been misidentified as white marlin [30-32]. The consequences of this misidentification include overestimation of white marlin populations and misunderstanding of both species’ biology, ecology, and harvest.

The paucity of ecological information, including population sizes, movements, and habitat use, for several billfish species is concerning since commercial and recreational fishing pressure remain intense. Improved ecological understanding from data gathered by satellite tags can be used to inform management strategies. Pop-up satellite archival transmitting (PSAT) tag studies studies have provided novel and crucial insights into the ecology of many marine organisms, especially large pelagic fishes (e.g. [3]). In the face of extensive declines of poorly understood, economically important billfish species, a thorough review is warranted to integrate the current literature on satellite tagging. Here, we conduct such a review to synthesize current knowledge on: (1) temperature, (2) light, (3) oxygen, and (4) complex water mixing as biophysical drivers of billfish behavior. In doing so, this analysis highlights the value of PSAT technology and the urgent need for further study on data-deficient species and better spatial coverage for currently studied species. We also contrast the effect of biophysical drivers on swordfish behavior with the istiophorid billfishes. Finally, we provide suggestions for future reporting of PSAT data in the literature to maximize the benefits of inter- and intra-specific data syntheses and comparisons.

Review

Approach and knowledge base

We performed Web of Knowledge and Google Scholar searches in September 2014 using topic and title searches for relevant keywords and common and scientific names for each species [e.g. topic = swordfish AND (“pop-up” OR “pop up”)]. Our search yielded 45 studies since 2001 that have employed PSATs to study billfish (Table 2), peaking at 7 per year in 2011. For those species studied extensively with PSATs, tagging efforts represented a comprehensive size range. Striped marlin, swordfish, and blue marlin dominate the focus of this body of work (cumulatively make up 70% of tag deployments), (Figure 1) while there were no published reports of PSAT studies on roundscale, Mediterranean, or shortbill spearfish. In addition, because roundscale spearfish were described only recently and came after the majority of studies occurred, the possibility exists that published white marlin data include those of roundscale spearfish. For simplicity and practicality, we refer to each species as it was originally identified and reported.

Table 2 Tag metadata for all billfish pop-up satellite tagging studies
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Figure 1
figure 1

Chronology of billfish pop-up satellite tagging publications. Cumulative frequency distribution of billfish publications over time for the seven species studied with this technology. Species abbreviations are listed in Table 1. Three species (MSP, RSP, SSP) have not been studied with PSAT tags.

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In order to synthesize and quantify overall billfish behavior, we first compiled a database of all published billfish PSAT data. We eliminated redundancy where several publications use the same individual datasets for different purposes (similar to the approach of [74]). We identified 1,082 unique satellite tag deployments yielding 824 unique tag datasets (Table 2). Individual datasets were only plotted in Figure 2 if tag and pop-up locations were given or enough spatial information could be found in the text or a published map to estimate individual displacement based on general tagging location (e.g. eastern Florida coast), overall heading, and mean straight-line distance (MSLD). With these criteria, we plotted 486 individual tag datasets (Figure 2) along with species-specific distribution data [15]. To date, tagging efforts have been concentrated in nearshore regions of Australia, New Zealand, and much of North America. These studies demonstrate displacement up to 5,970 km (mean 586 km, median 329 km) and deployments as long as 411 days (mean 62 days, median 41 days). The wide range in many of these study metrics is a product of the diverse objectives apparent in the reviewed body of literature. Many of the istiophorid studies are characterized by short-term tag deployments to assess post-release mortality, effects of hook type, and other fisheries-specific hypotheses (reviewed in [14,75]), whereas others seek insight into larger scale migratory behaviors.

Figure 2
figure 2

Movements of PSAT-tagged billfishes. Deployment (green triangles) and pop-up locations (red circles) of 486 billfishes in all pop-up satellite archival transmitting (PSAT) tag studies published between 2001 and 2014. Panels include locations for (a) 108 sailfish, (b) 119 blue marlin, (c) 184 swordfish, (d) 48 white marlin, (e) 2 longbill spearfish, (f) 20 striped marlin, and (g) 5 black marlin. Background polygons show species distribution, and color corresponds to species color in Figure 1. Panels h–j show distributions of shortbill, roundscale, and Mediterranean spearfish (respectively) that have yet to be studied with PSAT technology. Dashed polygons in panels f–g refer to spatial extent of 100+ and 42 tag datasets of striped (f) and black (g) marlin for which individual tracks could not be plotted (see note ‘p’ in Table 2).

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Biology

Movements and behavior are inherently coupled to species biology and ecology (e.g. trophic and environmental niches) and are directed by the physiological maintenance of homeostasis in the face of environmental variation [76]. As such, we first provide a brief overview of some of the few known biological aspects of billfishes in order to place our review of PSAT tagging data into the greater context of ecological and biophysical interactions.

In general, billfishes are obligate ram ventilators [77]; they must swim constantly to move oxygenated water over their gills, which have structural modifications that enable respiratory and swimming efficiency benefits. In addition, all billfishes maintain elevated eye and brain temperatures that facilitate cold water foraging without sacrificing visual and cognitive function [78,79]. Common food items among all species include small pelagic fishes and cephalopods [80]. Thorough larval collections in the Straits of Florida [81] indicate that spawning activity for the dominant istiophorids in the Atlantic (sailfish and blue and white marlin) generally occurs from April to October, while swordfish larvae have been collected year-round [81,82]. Other collections have identified billfish larvae from Hawaii, Gulf of California, and the Great Barrier Reef [61,83-85], most of which encompassed several months of the year.

Swordfish

Xiphias gladius have the broadest geographical distribution of all billfishes (Figure 2c) and are found worldwide from 45°S to 45°N [86]. Based on surveys of stomach contents, small pelagic fishes and squid are important prey items [87,88], and swordfish exploit their ability to maintain brain temperatures above ambient water to capture prey in cold, deep waters [89]. Swordfish in the northwest Atlantic appear to spawn primarily south of the Sargasso Sea and east of the Antillean Arc [90]. This may increase advection of larvae and early juveniles toward foraging grounds in the northwest Atlantic by the Gulf Stream [91]. Less consensus has developed in the Pacific, as studies suggest distinct north–south stocks [92], east–west stocks [71], and some stock structure within the western Pacific [93,94].

Blue Marlin

M. nigricans occupy tropical and temperate waters (45°S to 45°N) of the Indo-Pacific and Atlantic Oceans (Figure 2b). Like swordfish, blue marlin are able to forage at depth [23] largely on squid and small pelagic fishes [80]. They are believed to reach maturity at 2 years of age [95] and live up to 20 years [96]. Larvae have been identified near the Dominican Republic [38], the Bahamas [97], and the Florida Straits [46,81], co-occurring in these areas, respectively, with larvae of white marlin, sailfish, and both these species plus swordfish, suggesting that these regions are essential habitat for both spawning adults and developing larvae. Larvae and eggs have also been identified near Hawaii [83].

White Marlin

K. albida occupy temperate and tropical waters of the Atlantic Ocean and adjacent seas and are often found in areas of high food availability including fronts with and without flotsam and marked bathymetric features (e.g. banks, shoals, canyons) (Figure 2d) [98]. They are generally piscivorous, with prey specifically including dolphinfish, herring, and scombrids [80]. Seasonal movements between the northern coast of South America and the Mid-Atlantic Bight are common, and both trans-Atlantic and trans-equatorial crossings have been documented [99]. Spawning is thought to occur in at least five areas in the western North Atlantic, including the Gulf of Mexico, the Mona Passage (Dominican Republic), southwest of Bermuda, Little Bahama Bank near the Abaco Islands, and northwest of Grand Bahama Island [98]. Larvae have been identified in the Mona Passage [38], Florida Straits [81,100], and Gulf of Mexico [98].

Black marlin

I. indica primarily inhabits tropical and subtropical waters of the Indo-Pacific (Figure 2g) where it feeds on cephalopods, small tunas, and other fishes. Like other billfishes, black marlin make extensive seasonal migrations to high latitudes in summer months, where they occasionally occupy temperate waters, and return to low latitudes during winter in both hemispheres. However, only conventional tag data indicates extensive trans-equatorial and trans-Pacific movements [101]; thus, this behavior is still poorly understood. Along these routes, there is evidence of spawning in the South China Sea and Coral Sea, offshore of Taiwan, and near Cairns, Australia [11,61].

Striped marlin

K. audax is a highly migratory Indo-Pacific species found throughout tropical and temperate waters (Figure 2f). It is believed to have a unique distribution among billfishes in the Pacific that stretches from the northwest Pacific to the eastern and southwest Pacific in a horseshoe shape [11]. Shimose et al. [102] suggest that striped marlin migrate between open-ocean feeding habitats and nearshore spawning areas in Hawaii [84] and in the Gulf of California [85]. Limited PSAT data for this species support this migration hypothesis and suggest regional site fidelity in some areas [7]. K. audax is mainly piscivorous and has been shown to feed on a variety of taxa including Molidae, Ostraciidae, Scombridae, and others [102].

Sailfish

I. platypterus is found worldwide in tropical and subtropical waters and is unique amongst the billfishes in its association with near-coastal waters over shallow continental shelves, although catch records suggest a nominal presence in some offshore regions of the tropical Atlantic (Figure 2a) [103]. Larval densities suggest spawning at front edges in the Florida Current [104], and Simms et al. [105] found the highest larval densities at convergent fronts in the northern Gulf of Mexico created by freshwater input and current convergence.

Longbill Spearfish

T. pfluegeri is a rare, relatively small istiophorid with a primarily offshore distribution. It occurs in the Atlantic Ocean and adjacent seas from Georges Bank to South Africa (Figure 2e) [50]. These fish are visual predators that likely feed primarily during the day [106,107] on epipelagic prey [80]; however, little else is known about the biology of this species.

Roundscale Spearfish

T. georgii is widely distributed (Figure 2i) and was initially thought to largely inhabit the western North Atlantic [25,108]. While it was recently found in the central North and South Atlantic [30], no PSAT studies have been conducted to confirm movements within or among these areas. Though somewhat cryptic, the validity of the species among the spearfishes (Genus: Tetrapturus) has been confirmed [12,32]. However, the recent realization that roundscale spearfish have often been characterized as white marlin has led to uncertainty in the collective knowledge of both white marlin and roundscale spearfish—especially since roundscale spearfish may be more abundant than white marlin at particular times in some areas of the North Atlantic [25,31]. In general, however, aside from morphological information from confirmed roundscale spearfish specimens [25], there is, as of yet, little biological or ecological information available for the species.

Mediterranean spearfish

T. belone has the most limited distribution of all spearfishes as it is largely restricted to the Mediterranean Sea (Figure 2j), but occasional catches in the Atlantic have been reported [26]. Although not a target species for most fisheries, it is caught by harpoon in the Straits of Messina, where it is also known to reproduce [26]. Analysis of stomach contents suggests that pelagic fish and cephalopods comprise the diet of this species [109,110]. However, no reports of satellite-tagged Mediterranean spearfish were found, and there is little other information available about the movements and habitat preferences of this species.

Shortbill spearfish

T. angustirostris is a widespread (Figure 2h) but rare, data-deficient species that inhabits tropical to temperate waters of the Indo-Pacific. This species is generally found above the thermocline and well offshore, rarely entering coastal waters (Figure 2h). They are mainly piscivorous and primarily feed on Molidae [102], crustaceans, and cephalopods [11]. Shortbill spearfish eggs have been identified in the equatorial western Indian Ocean [111] and near Kona, Hawaii [83].

Biophysical drivers

Temperature

Temperature controls biochemical reactions and metabolic rates of fishes [112] and is arguably the best understood and most influential environmental variable driving billfish behavior and distribution. PSAT studies for all billfish species report high occupation of narrow thermal regimes with some inter-specific variation in magnitude and range. Most billfishes appear to be largely confined to the warmer side of the 22°C–24°C isotherm [21,34,38,47,50]. In one study, the majority of blue marlin tagged near Bermuda spent >75% of their time in the upper 10 m of the water column where they experienced water temperatures >26°C [21]. Near the Dominican Republic, individuals spent at least 50% of their time in the top 25 m and up to 75% in temperatures 28°C–30°C [38]. Blue marlin tagged in the Caribbean spent more time in cooler waters during the day than at night, with some fish briefly entering waters cooler than 10°C [41]. Similar depth occupation is reported for the slightly smaller white marlin along the United States. Atlantic coast south to Venezuela [38,58]. Sailfish are among the most surface oriented of the billfishes, spending over 80% of their time at surface temperatures during the day and 93% at night in the Atlantic, which is consistent with the behavior reported for sailfish in the Pacific [63,72,73] and for the only two longbill spearfish that have been tagged [50]. Black marlin in the Coral Sea were found to occupy shallow waters warmer than 24°C [60], and their horizontal movements correlated with the spread of 26°C–27°C sea surface temperatures (SST) [61]. Striped marlin are also largely surface oriented, spending 80% of their time in the mixed layer and 72% in the top 5 m [66]. Collectively, heavy use of the surface and mixed layer suggests that a subsurface temperature barrier plays a key role in determining billfish vertical behavior [21,34,58].

Swordfish are the most vertically active billfishes. They typically follow the >22°C isotherm trend during nocturnal occupation but deviate considerably during daytime hours, when they inhabit the upper mesopelagic region (8°C–16°C) before returning to the surface again at sunset, e.g. [55]. This use of a cooler, deep layer may contribute to the occasional and brief daytime basking behavior commonly observed in swordfish tagging studies [54,70].

Diel depth and, consequently, temperature differences are driven by a combination of factors including thermal inertia relative to an individual’s body mass, cardiac limitations, neural warming, foraging opportunities at depth, and light availability required by these visual predators [41,113,114]. Data are currently unavailable on the diel variability of prey consumption for most istiophorids and specifically whether a nocturnal behavioral change is related to feeding; however, variation in swordfish diets has demonstrated predation on deep scattering layer (DSL) organisms [115]. Some studies show epipelagic tuna and billfish species are limited to temperatures within approximately 8°C of SST (e.g. [48,63]) because of the effects of temperature on cardiac function; deeper dwelling tunas and swordfish compensate for their activity in cooler, low-oxygen, subthermocline waters via specific physiological adaptations in their cardiorespiratory system [116-118]. In epipelagic tunas, poor cardiac calcium cycling causes excitation-contraction coupling to break down in cardiac myocytes when instantaneous temperature changes exceed a roughly 8°C instantaneous range [118,119]. Similar processes are presumed to occur in istiophorid hearts [114,116]. Accordingly, forays to depth must be brief and cardiac muscle must thereafter be warmed, resulting in a vertical movement pattern reminiscent of an air-breathing vertebrate in which vertical excursions are followed by surface “recovery” periods [58]. Body size and consequent thermal inertia (i.e. how long the fish retains the heat gained from occupying the mixed layer) influence the variation in dive depths and ambient temperatures that is often observed among individuals and between species [41,48,120]. In contrast, deeper dwelling pelagic fishes, such as swordfish and some tunas, forage extensively below the mixed layer by maintaining cardiac function via greater capacity for cardiac calcium cycling at reduced temperatures [118,121]. Selective heating of the neural infrastructure of the brain and eyes in billfishes and tunas also contribute to their ability to conduct sustained forays into cold water [78,89,122] and provide superior vision for deep foraging [79]. Additionally, surface basking may be a behavioral mechanism for thermoregulation [54,70].

Light

As visual predators, istiophorids and swordfish require adequate ambient light for image formation and foraging. Disproportionately large eyes are characteristic of all billfishes and, combined with selective heating of neural infrastructure as mentioned above, increase the ability to form and neurally process images of moving prey [79]. These adaptations are thus thought to increase prey capture success in cold, dark waters during the day and in the moonlit surface layer at night [68,123]. Consequently, large vertical excursions often occur during daylight periods when illumination at depth is greater.

Swordfish vertical movement is strongly related to light penetration in the Atlantic [52,54,124], Pacific [54,68,70], and Mediterranean Sea [125]. Specifically, maximum daytime depth is significantly correlated with light penetration, and nighttime depth has been shown to increase during the full moon, suggesting that swordfish are feeding on deep scattering layers at depth during the day and vertical migrators in the upper water column at night [52,54,55]. Their large eyes likely provide significant benefits for prey capture in low light conditions [79], and, as such, this species is generally exposed to very limited solar illumination except when basking during the day [54,70].

Although istiophorid billfish also have large eyes that are presumably similarly advantageous in low light conditions, most evidence indicates they are largely surface oriented, especially during daylight hours. Blue marlin spend the majority of time at the surface [23] while making occasional foraging trips below 50 m and give little indication of diel differences in behavior [37,39]. Sailfish exhibit marginal diel changes in vertical movement behavior [48,49,73], with some reports of increased vertical activity during the day than at night [64]. No diel changes are apparent for black or white marlin, aside from occasional qualitative observations of the latter that only persisted for short periods of the tag records [58,60]. While striped marlin in the southwest Pacific largely occupied the top 5 m, they spent significantly more time below 100 m during the day than at night [66]. Thus, although equipped with seemingly adequate vision for deep daytime foraging as observed in swordfish, istiophorids exhibit limited deep foraging behavior presumably due to a subsurface temperature barrier and physiological limitations of functioning in cold water (see section “Temperature” above) .

Oxygen

Dissolved oxygen (DO) also has a substantial influence on billfish behavior and distributions because at low levels it constrains maximum metabolic rates and, thus, metabolic scope [112]. Regions of low dissolved oxygen occupy nearly all of the equatorial Atlantic and eastern tropical Pacific [43,126], and the volume, extent, and severity of these zones are expected to increase with climate change [127]. Although little direct support is available from satellite tags due to their inability (until recently) to measure DO in the water column, compelling evidence exists for some tagged individuals. For example, two longbill spearfish tagged in the South Atlantic appear to have been deterred from areas with DO <3.5 mL L−1 [50]. Furthermore, the mean daily maximum depth of two blue marlin doubled when they left the oxygen minimum layer (OML) region of the eastern tropical Atlantic [43]. Both blue marlin and sailfish occupied the surface layer more extensively in the eastern tropical Atlantic than in the northwestern Atlantic where they traveled deeper and utilized greater depths more often. This behavior correlated with the presence and extent of OMLs that presumably constrained vertical habitat in the eastern tropical Atlantic [43]. As obligate ram ventilators with high metabolic demand and, by extension, high oxygen consumption [128], it is unlikely that billfish can remain in hypoxic waters for an extended period before they incur oxygen debt and require greater DO levels. This may drive avoidance of waters with low DO [129]; however, Dewar et al. [54] report that all 31 Pacific swordfish in their study experienced oxygen levels below 2.15 mL L−1, and Abecassis et al. [70] demonstrate that swordfish can endure severe hypoxia (<0.2 mL L−1). The apparent ability of swordfish to tolerate low DO compared to istiophorids may be at least partially due to differences in gill surface area. Branching of distal gill filaments resulting in an increased number of secondary lamellae is characteristic of swordfish but not found in istiophorids [130]. Blood oxygen binding may also play a role in DO tolerance in billfishes, but its role is thus far unknown.

Current climate change predictions suggest that eutrophication-derived coastal hypoxia and large-scale declines in oxygen levels of tropical waters will result in as much as a 7% decrease in global ocean oxygen content [131,132]. As ocean oxygen content declines and OMLs continue to grow [126], there will be increased habitat compression in both the vertical and horizontal dimensions [120,127]. Stramma et al. [127] suggest that between 1960 and 2010 around 15% of billfish habitat in the upper ocean layer of the tropical northeast Atlantic has been lost to OML expansion. As this expansion continues, restriction of vertical habitat will concentrate billfishes in the surface layers of the Atlantic. At the same time, prey concentrations subject to the same conditions also gather at the surface, which could allow increased billfish growth as a result of increased feeding opportunities and caloric intake. Indeed, Prince and Goodyear [120] hypothesize that sailfish are larger in the eastern Atlantic than in the western Atlantic as a result of habitat compression and increased feeding opportunities. However, with loss of vertical habitat, these fish will be more vulnerable to exploitation by fishing gear [43,120]. Thus, an already overexploited group may experience heightened pressure in the future as available habitat with sufficient oxygen continues to decline, concentrating both prey and fishing effort.

Complex water mixing

Submeso- and mesoscale features are also hypothesized to be a main driver of billfish distributions and behaviors [91]. For example, satellite tracking of swordfish off the southeastern coast of the U.S. showed that these fish were attracted to areas with high-relief bottom structure and the complex thermal structure of fronts that emerge when warm Gulf Stream water meets colder shelf and slope waters near the Charleston Bump [51]. Four of 29 tagged fish stayed in the vicinity of the Bump for extended periods of time where numerous thermal fronts are generated by Gulf Stream deflection and upwelling. Those fish that moved away occupied regions above submarine canyons and seamounts, which also exhibit complex oceanographic processes. Supporting these results, catches of swordfish are high along frontal regions in the Mid-Atlantic Bight off southern New England where Labrador Current waters interact with the Gulf Stream [133], and PSAT data indicate swordfish frequently occupy and traverse this region (Figure 2c). High riverine nutrient inputs also lead to enhanced production along fronts and is often coupled with enhanced frontal upwelling in regions like the Mississippi [134,135] and Amazon river plumes [136], both of which are places of concentrated blue marlin catch [44] and high-density PSAT data (Figure 2b) in the Atlantic.

Larval billfish may have an even stronger relationship with frontal structures as they are often found in the vicinity of major frontal zones and other oceanographic features [137]. Fast growing billfish larvae, which are found in low-latitude, oligotrophic regions with high sea surface temperatures, need concentrated food to fuel their high metabolic demands, and spawning at fronts would serve as a strategy to reduce (even if slightly; cf. [138]) the high-mortality larval phase and increase spawning success. Several regions (mostly in the western North Atlantic) have evidence of relatively high larval densities [38,81,139]. Larval age estimates indicate that adult sailfish spawn during eddy formation, presumably to ensure larvae are retained within a relatively food-rich environment while they develop [104]. An additional, but related, mechanism was proposed by Mourato et al. [140]. The authors describe a dramatic shift in wind direction off the southeastern Brazilian coast during summer that drives strong coastal upwelling and a large intrusion of nutrient rich water onto the continental shelf. This shift often coincides with high adult sailfish densities in the region (although thus far unsupported by PSAT data; Figure 2a) and may constitute an important temporary food source for sailfish larvae. Thus, these areas may provide critical spawning habitat for some large pelagic species [137].

Although there is evidence for billfish association with complex physical features, the technological limitations inherent in PSAT technology (namely, large uncertainty in position estimates) preclude robust, quantitative associations between large pelagic fishes and meso- and submesoscale features. PSAT tags are capable of providing purely objective measurements of biophysical relationships, but several studies demonstrate that conventional light-based geolocation techniques are inadequate due to large spatial error [141,142]. Higher resolution methods are now becoming available [69,143] and should facilitate rapid improvements in this field.

Conclusions

Biophysical interactions

To date, over 1,080 tags have been deployed on billfishes worldwide. Although much of this effort assessed post-release survival (notably the effect of hook type and bycatch mortality) and vulnerability to various fishing gear types with short tag deployments, these studies collectively represent a substantial dataset for drawing inferences about billfish biology and ecology. In this review, we synthesized available information to explain the main biophysical factors influencing billfish distribution and behavior. Many tracked individual billfishes spent significant time in the warm surface layer suggesting a strong thermal utilization of waters >22°C. However, swordfish in particular demonstrate repeated deep vertical movements that suggest foraging at depth where their greater thermal inertia, large eyes, and ability to selectively warm their eye and brain tissues may allow them to maximize capture efficiency and make these movements energetically favorable. Some evidence suggests waters with low dissolved oxygen can influence billfish distribution and movements; however, swordfish appear uniquely capable of associating with low dissolved oxygen concentrations. Tagged billfish also demonstrate considerable occupation of frontal regions that may provide increased adult and larval feeding opportunities and could elicit decreased larval mortality. Current climate change predictions indicate that low oxygen zones will increase in size, which may lead to further habitat compression and thus increased vulnerability of these species. Additionally, species ranges may shift as a result of predicted ocean warming [144].

Future directions and recommendations

Future research efforts and funding paradigms should focus on designing and supporting studies with explicit ecological hypotheses that link PSATs to integrated and real-time oceanographic technologies. This is a grand challenge as PSATs are expensive and studies using them have often been funded to address specific applied management concerns. Specifically, studies should focus on hypotheses related to changing distribution patterns as a result of environmental shifts. For example, understanding whether billfish range expansions are occurring as a result of changing temperature and prey distributions is a key ecological question that PSAT studies could address. Additional PSAT tag deployments will be similarly critical for quantifying the effects of low DO on billfish biology and the implications of future climate scenarios for these species. To this end, new PSAT tag technologies will facilitate both high-resolution locations to understand fine-scale biophysical interactions (e.g. front association) and in situ DO measurements on tagged individuals.

Integration of large volumes of oceanographic data (e.g. ARGO float program) with animal-borne tag records will enable a better understanding of both billfish ecology and oceanographic patterns, especially when one considers that tag-bearing fish are essentially autonomous samplers of the water column. The collective synthesis afforded by such an approach is critical for designing effective management strategies and sustainable harvest. In addition, efforts should be made to expand PSAT deployment to some of the little-studied billfish species (e.g. longbill, roundscale, shortbill, and Mediterranean spearfishes) and those with poor spatial coverage (Figure 2). Improved metrics for species identification should facilitate disambiguating white marlin and roundscale spearfish and allow directed study on each species.

Finally, after extensive review of the PSAT literature, we propose three recommendations from which future comparisons and syntheses could benefit. Specifically, we suggest: (1) if a tag dataset is analyzed or reported on in publications subsequent to its initial publication (e.g. addressing different questions), this should be stated clearly to avoid confusion and facilitate synthesis across studies; (2) reporting a thorough description of tag data and metadata for each tag deployed (when possible) that includes tag identification number (serial, platform terminal transmission, etc.), tag type, deployment and pop-up locations and dates, fish size and sex, days at liberty, depth range, temperature range, and bins used for depth and temperature summary data; and (3) publishing depth and temperature bin data (e.g. time spent in programmed depth intervals) to facilitate comparison among studies and taxa. Most journals allow online supplemental material at no additional cost. This is the perfect venue for publication of additional tag metadata that would further enable synthesis across studies.