Understanding the spawning strategies of large pelagic fish could provide insights into their underlying evolutionary drivers, but large-scale information on spawning remains limited. Here we leverage a near-global larval dataset of 15 large pelagic fish taxa to develop habitat suitability models and use these as a proxy for spawning grounds. Our analysis reveals considerable consistency in spawning in time and space, with 10 taxa spawning in spring/summer and 9 taxa spawning off Northwest Australia. Considering the vast ocean expanse available for spawning, these results suggest that the evolutionary benefits of co-locating spawning in terms of advantageous larval conditions outweigh the benefits of segregated spawning in terms of reduced competition and lower larval predation. Further, tropical species spawn over broad areas throughout the year, whereas more subtropical and temperate species spawn in more restricted areas and seasons. These insights into the spawning strategies of large pelagic fish could inform marine management, including through fisheries measures to protect spawners and through the placement of marine protected areas.
Large pelagic fish, such as tuna and billfish, are key species in marine food webs. They are important socioeconomically, supporting valuable fisheries in subtropical and tropical national waters and in the high seas. These fisheries provide income and food for many countries, particularly island nations of the Global South. Many large pelagic fish also play important ecosystem roles in carbon cycling through predation, diel vertical migration, and sinking of feces and carcasses. Their high mobility, migrating across vast ocean expanses and traversing both national boundaries and the high seas, presents challenges for their effective fisheries management and conservation. A deeper understanding of their life history -- including how these species reproduce in time and space -- could ultimately aid their management.
Life history strategies of pelagic fishes are highly variable and can be inferred from co-variation in traits, such as body size, longevity, growth rates, and fecundity. In scombrid fishes (tunas, bonitos, mackerel), most life history variation is explained by traits describing body size, swimming speed, and reproductive schedule, with body size being the most influential. At one end, opportunistic strategists, such as tropical tunas (e.g., skipjack tuna - Katsuwonus pelamis), have a fast life history strategy. These species are often small to medium in size, grow rapidly, mature early, and have short life spans. At the other end, periodic strategists (e.g., Atlantic bluefin tuna - Thunnus thynnus) predominantly inhabiting temperate waters have a slow life history. These species are often large in size, grow slowly, mature late, and have long life spans, leading to slower population turnover. Similarly, billfishes such as marlin, spearfish (Istiophoridae) and swordfish (Xiphiidae), also have a slow life history strategy because they are large bodied, late-maturing and slow-growing.
Fundamental to the life history strategy of large pelagic fish is their spawning strategy in time and space. Tropical scombrid species with a fast life history generally have a longer spawning season than subtropical and temperate scombrids with a slow life history. Although, it is unknown whether this trend is followed more generally by other large pelagic fish. By contrast, there is much more limited information on the extent of spawning grounds of large pelagic fish in relation to life history variation. Muhling et al. interestingly noted the tendency for three bluefin tuna species with slow life histories to spawn in spatially restricted spawning grounds. A synthesis of the spawning strategy in time and space of large pelagic fish could provide valuable insights into evolutionary processes governing spawning. Many species tend to return to one or several natal grounds to spawn at similar times each year. For example, some spawning grounds host aggregations of multiple large pelagic fish species, such as off Northwest Australia for skipjack and Southern bluefin tuna, and off Japan for skipjack and Pacific bluefin tuna. This co-location of spawning is despite these species having contrasting life history strategies. The extent to which this strategy of co-location of spawning in space and time is prevalent among a broader suite of large pelagic fish taxa remains unknown.
The best data on near-global spawning dynamics is restricted to key commercial tuna and billfish species, with limited information for other non-targeted species. Multiple studies have found restricted temperature preferences for large pelagic fish, suggesting co-location of spawning. Reglero et al. found that seven tuna species preferred spawning in warm waters and Schaefer found that tuna species spawn in waters >24 °C. Muhling et al. suggested that tuna larvae tend to be found within narrower temperature windows than adults, suggesting that there could be considerable overlap in larval distributions. Reglero et al. also found that most tuna spawned in waters of intermediate values of mesoscale activity from eddies, supporting the triad hypothesis of Bakun (2006) that links favorable spawning areas to the physical environment, and suggests that co-location might be a valuable strategy. This evidence for common environmental drivers of many species and the co-location of their spawning in time and space indicates that large pelagic fish could exploit advantageous environmental conditions for adults and larvae.
There could also be substantial evolutionary benefits for large pelagic fish species if their spawning is segregated in time and space. This could reduce density-dependent food limitation and thus competition for food by adults, potentially increasing spawning and enhancing recruitment. Such segregated spawning could also enhance the food availability for developing larvae, reduce egg and larval cannibalism by conspecifics, and decrease predation on eggs and larvae by other large pelagic fish species and invertebrates, all of which could lead to an increase in survivorship, a major factor limiting recruitment. Therefore, both strategies -- species either segregating or co-locating spawning in time and space -- could have evolutionary benefits for large pelagic fish species.
A deeper understanding of the variation in life history strategies of large pelagic fish could provide the foundation for their improved management. For example, if many species co-locate their spawning in time and space, then this could be used in fisheries management to help avoid harvesting spawning females and to elucidate stock structure. Detecting co-located spawning grounds, could also inform the location of marine protected areas (MPAs) or other effective area-based conservation measures (OECMs). Although debates persist on the potential benefits of MPAs for highly migratory fish species and challenges exist in protecting such species throughout their long migrations, species such as tunas and billfish are likely to receive some benefit from the protection of their spawning areas. As countries seek to meet the Global Biodiversity Framework target of conserving 30% of land, waters and seas by 2030, knowledge of the spawning areas of commercial and non-commercial species are likely to be valuable, especially considering the lack of data available for pelagic ecosystems.
Assessing the spawning strategies in time and space is complicated by the paucity of available data. Collecting spawning data during field surveys is labor-intensive and expensive. It usually involves sampling individual females to assess gonadal state or eggs and larvae from the water column and is sometimes complemented by local knowledge and observations. Realized spawning areas -- defined by the presence of eggs -- are difficult to identify because they are patchy and ephemeral, particularly for highly migratory species. For these species, the presence of larvae is often used as an indicator of spawning events. Larval data and habitat suitability models can then be used to identify potential spawning times and locations. Most data on the larvae of large pelagic fish species are collected from one-off surveys, involve individual species, cover local-to-regional scales, and use different methods. A notable exception is the extensive dataset of Nishikawa et al., which provides an unprecedented window into the spawning strategies of large pelagic fish species. This data set spans 40°N to 40°S at 1° × 1° resolution, includes seasonal data collected during surveys from 1956 to 1981, and has 63,017 samples collected with similar methods. The seminal work of Reglero et al. on environmental requirements for spawning habitats also used the Nishikawa et al. observations and other data sets at a coarser resolution (5° × 5°) and investigated seven tuna species. However, they did not assess spawning seasonality, nor did they address the question of the co-location of spawning by different species.
Here we leverage previously digitized larval data as a proxy for spawning to answer questions about the generality of spawning strategies -- over time and space -- for 15 taxa of large pelagic fish of both commercial and non-commercial value. We match these larval data with environmental variables from Earth System Model (ESM) outputs to build larval habitat suitability models and thus identify potential seasonal larval hotspots in the Indian and Pacific Oceans. To provide insights into spawning strategies, we assess the degree to which larvae for multiple species are segregated versus those that are co-located in hotspots across time and space. We investigate how consistent these spawning patterns are across hemispheres and across a slow-fast continuum of life history strategies. Finally, we test the influence of latitude -- specifically, whether the spawning season of large pelagic fish is longer and their spawning grounds are more restricted spatially at higher latitudes than those at lower latitudes. This work could help inform conservation and sustainable use of these large pelagic fish, through informed fisheries management measures and protected area placement.