Fish population growth depends on older mothers, which in some species produce more and ‘better’ offspring than younger fish. When fisheries remove the most productive females, the whole population suffers.
English literature about the ocean is predominantly male. Ernest Hemingway's The Old Man and the Sea was about an aggressive fight against the elements and the imponderable deep, with the main protagonist being the masculine el mar. But the real state of fisheries depends more on the role of females in the replenishment of fish populations. As Steven Berkeley and colleagues1 now report in Ecology, that role has surprising facets. They find, contrary to popular wisdom, that in the black rockfish, older, larger female fish produce eggs and larvae that are much more likely to survive. From the standpoint of population growth rate and the potential to recover from overfishing, the old saying and country-and-western lyric may apply more often than Hemingway: “If Momma ain't happy, ain't nobody happy.”
Larger female fish are vastly more productive than their smaller sisters. A single 61-cm-long red snapper (Lutjanus campechanus) has been estimated to produce as many eggs as 212 43-cm-long snappers2. This is largely because eggs are produced in proportion to a fish's volume, which is proportional to the cube of its length. The profligate fecundity of larger females has long been cited as a good reason to preserve fish populations in ‘no-take’ marine reserves. In some cases, larger fish in these reserves may double a species' egg production — even if the reserves encompass only 5% of the marine habitat3.
Berkeley and co-workers1 have documented another benefit from larger, older females. They studied rockfish of the genus Sebastes (Fig. 1), and found that eggs from older females produced larvae that grew faster and were more resistant to starvation than larvae from younger females. The differences were huge: on the same diet, larvae of 12-year-old rockfish grew four times faster than larvae produced by 5-year-old rockfish. At the same time, offspring of older females had more metabolic reserves: larvae took an average of 12 days to starve whereas offspring of 5-year-olds starved in less than half that time.
The central difference lies in a small post-hatching gift each mother gives her offspring, a little oil droplet that serves as a metabolic reserve after the yolk-sac has been absorbed (Fig. 2). Older females provide a larger droplet than younger ones, ensuring a better head start for their larvae as they drift through the oceans, feeding and developing into juvenile fish capable of settling to the sea floor. Larger females, and females in better physical condition, produce better larvae as well, but these effects are slight compared with the effects of age. Such observations are particularly surprising in light of long-held views that the optimum reproductive allocation per offspring should be independent of age or parent size4. Berkeley and colleagues are not sure why age makes such a difference, but there may be hidden age-related shifts in reproductive effort that will eventually provide an explanation.
These data are also important for attempts to rebuild overfished rockfish populations. Fishers value larger, older fishes — remember Hemingway — and strip away these larger individuals from the reproductive populations. In other fish, such as grouper species that change sex from smaller females to larger males, this tendency to take larger fish has long been known to reduce the number of mature males. Some grouper spawning aggregations have fewer than one male for dozens of females5, and this imbalance exhausts the fertilization abilities of the few surviving males. The opposite problem is seen in shrimp and crab populations where small males change into larger females6. Fishing down the family tree in these cases removes females first, and cuts egg production dramatically7.
The new data show why heavy fishing pressure on older fish is also a serious problem in species that don't change sex. For example, in coastal Oregon, Berkeley and colleagues1 document a decline in the average age of female rockfish from 9.5 years to 6.5 years during a period of intensified bottom fishing from 1996 to 1999. Such a culling of the older females reduces the average growth rate of larvae in the population by about 50%, and probably reduces the ability of these larvae to grow and survive to the next stage in their life history. Data on cod and haddock also show that larger females produce larger eggs: presumably these larger eggs produce better larvae8,9. The conclusion is that standard fisheries management tools that consider every female to be reproductively equivalent can be far off the mark.
Marine reserves change the landscape of fishing regulations by protecting the entire local populations of fish and invertebrates. The resulting dramatic reduction in mortality has an immediate benefit in producing larger fish in reserves — an effect that has been seen in tropical and temperate settings, along reefs, kelp beds and in estuaries. So protecting larger, older females can be more efficient in producing larger numbers of higher-quality offspring. Not all fisheries suffer from the need for more offspring. But because reproduction is the fuel that keeps all fisheries alive from one generation to the next, enhancing the success of larvae is a key to a sustainable fisheries future.
And Hemingway's Old Man Santiago may have known the power of females in the sea all along. Younger fishermen thought of the sea as masculine: “But the Old Man always thought of her as feminine and as something that gave or withheld great favours”10. Those favours are written in the next generation of the sea's creatures, and these new research results tell us that it is the favours of the mothers that matter most.