Fishing out a feeding paradox

If an animal’s body shape is specialized in a way that aids feeding on specific organisms, does this restrict what the animal can prey on? An observation of fishes feeding in the wild might now help to settle this question.
Sebastian Kruppert is in the Department of Biology, Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington 98250, USA.

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Adam P. Summers is in the Department of Biology, Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington 98250, USA.

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A chance observation of fish behaviour, made during an underwater survey along the eastern shore of Lake Tanganyika in Tanzania, has now been reported in American Naturalist by Golcher-Benavides and Wagner1. Their observation neatly ties together 40-year-old laboratory data2 and a model of evolution based on an idea known as optimal-foraging theory3.

The serendipitous event occurred when Golcher-Benavides was on a dive with a Tanzanian colleague, George Kazumbe, studying the species present in a region perpendicular to the lake’s shoreline. They saw ahead, sparkling between the lake’s surface and its rocky bottom, a massive school of juvenile sardines, estimated to comprise at least 50,000 individuals. Video footage of this event captured what happened when the sardines encountered fishes belonging to a group called the cichlids.

There are about 250 species of cichlid fish in Lake Tanganyika4. These species represent fishes that have a wide variety of feeding specializations, including those that have evolved in a way that allows them to target a single type of prey57, as well as fishes that are capable of eating diverse sources of food. The shapes and features of the heads of some cichlid species bear witness to the adaptation that is suited to their particular food source (Fig. 1).

Petrochromis polyodon and Haplotaxodon microlepis

Figure 1 | Cichlid fishes. Some species of fish belonging to a group called the cichlids have body-shape specializations that help to capture specific types of prey. For example, Petrochromis polyodon (a) has large lips, which enable this species to scrape algae from rocks, whereas Haplotaxodon microlepis (b) has an upward-oriented mouth that is suited to feeding on zooplankton floating in the water. It has been debated whether cichlid feeding specialists eat only the food that they have evolved to target. If specialists can still target a variety of food sources, this poses the condundrum, termed Liem’s paradox, of how such specializations evolve. Golcher-Benavides and Wagner1 report an observation of wild cichlids, including the species shown, that encountered a school of sardines they are not specialized to feed on. P. polyodon did not eat the sardines; however, H. microlepis switched from its usual food source to eat the sardines.Credit: (Left) Melchior de Bruin; (Right) Evert van Ammelrooy

One example of a cichlid species that has evolved a feeding specialization is Perissodus microlepis. This fish has a curved head, and when it swims alongside a larger fish, it can suddenly attack and snatch a mouthful of scales8. The population of this species is split between fish whose head is curved to the left for attacking the right side of its fish prey, and fish whose head is bent rightward to enable an assault on the prey’s left side. Other cichlid feeding specializations include those for scraping algae from rocks9, biting out the eyes of other fish10, and gobbling eggs knocked out of the mouths of brooding parents11.

It was thought that these feeding specializations allowed specific food sources to be targeted as a way of handling intense competition for food. However, during the late 1970s and early 1980s, the biologist Karel Liem made some muscle recordings of cichlids during prey capture in the laboratory2. These showed that some specialized cichlids retain the capacity to make the movements necessary to capture a range of prey. Liem therefore asserted that it was a paradox (now referred to as Liem’s paradox) that a fish best suited to a single type of prey could be a jack-of-all-trades.

But if specializing carries no penalty in terms of limiting the type of food a fish can eat, there should be little competition-driven need for specialization. Liem’s paradox was met with scepticism, because it seemed to contradict a basic principle of evolution: ecologists view competition for food as a key driver of evolutionary processes of selection.

To try to resolve this debate, evolutionary biologists Beren Robinson and David Wilson developed a mathematical model3 describing how feeding specialization might offer a competitive advantage. Their modelling suggested that rare periods of food scarcity could drive the evolution of a body form that has a specialized feeding capacity, while leaving intact the ability to eat other commonly available, easy prey. This hypothesis, based on optimal-foraging theory, shows how competition could still have a role in explaining Liem’s paradox. It made a distinction between versatility and specialization — even though a certain head shape evolved during natural selection to target a specific type of prey, this head shape might still function well to capture a wide range of easy prey.

Robinson and Wilson’s theoretical framework provided a crucial insight into Liem’s paradox, and it is consistent with evidence indicating that the diets of fishes that differ in their form can still broadly overlap12. However, there is an asymmetry in the trade-offs between food handling and competitiveness: gaining the capacity to target a low-payoff dietary item might cost little in terms of eating high-payoff, easy prey, but if such a change resulted in loss of the ability to eat easy prey, it would be expensive for the predator. The fingerprints of evolutionary selection on the shape of a fish’s head should reflect the need to acquire the rare food items that get a species through adverse times, not items that represent food staples or windfalls.

How well do these theories reflect what happens in the wild? Only limited results have been reported so far. For example, there is evidence that the diets of two cichlid species of algal scrapers include more than just algae13. Golcher-Benavides and Wagner’s report now provides comprehensive evidence of what happens when specialists encounter easy and abundant prey, in the form of sardines, that they are not specialized to eat. The researchers estimated that around 870 cichlids from 31 species fed on the sardines. The cichlids had abandoned the prey on which they are specialized to feed in favour of these easy pickings. Some of the cichlids that the authors observed — which might normally eat only fish scales or eyes, or the biofilms (made of organisms such as bacteria and algae) that collect on submerged rocks — feasted on sardines by reverting to their juvenile, suction-based mode of feeding.

The cichlids identified in the encounter with the sardines fell into ten groups, corresponding to their typical mode of specialist feeding. Fishes from eight of the groups enthusiastically attacked the sardines, but cichlids in two groups seemed to have made too great a trade-off in specialization and missed out on the feast. In particular, cichlids that had a strongly downward-facing mouth or ‘tricuspid’, alga-combing teeth didn’t take the sardine snack.

This single observation gives field-based support for a theory that sprang from experimental observations. It also demonstrates the importance of the well-trained and mentally prepared naturalist who can fit real-world observations into a framework that encompasses the scientific literature and personal experience.

Nature 571, 181-182 (2019)


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