Kelp consumption curtailed by señorita

Miranda Haggerty was diving through a kelp forest, and noticed that many kelp bore a large number of tiny limpets that were housed in small scars that they (or a fellow-limpet) had excavated on the kelp’s surface. This got her thinking about how these scars might affect the kelp, and equally relevant, whether there were any limpet predators that might lend the kelp a hand (or a mouth) by removing limpets.

Jerry Kirkhart

A limpet grazes on a kelp frond. Credit: Jerry Kirkhart

Feather boa kelp (Egregia menziesii) is a foundation species within the subtidal marine system off the California coast, providing food and habitat for many species that live on or among its fronds. The tiny seaweed limpet, Lottia insessa, specializes on feather boa kelp, grazing on its fronds and living within the scars. Many invertebrates and fish live within the kelp forest, but the most abundant fish is the señorita, Oxyjulis californica. Haggerty wondered whether the señorita might benefit the kelp (directly) by removing limpets, or (indirectly) by scaring limpets away – what ecologists call a trait-mediated indirect interaction.


The señorita – a fearsome predator of limpets.  Credit: Miranda Haggerty

The first order of business was to determine whether the limpets were actually harming the kelp.  Haggerty and her colleagues approached this in two ways.  First they chose 94 kelp plants from kelp forests off the California coast.  From each individual they chose one grazed and one ungrazed frond (each 3 m long). Grazed fronds averaged 5-10 scars and at least 2 limpets per meter of length.  Every three weeks they visited their kelp to score for broken fronds. In 29 of 30 cases, the grazed frond broke before the ungrazed frond (in the remaining cases the entire plant was missing, or both fronds broke and the researchers could not tell which had broken first).


Photo of feather boa kelp showing grazing scars, including one housing a limpet (left).  Diagram of feather boa kelp showing multiple fronds (right).

But the researchers were concerned that perhaps limpets chose to graze on weaker fronds, so the breakage was not caused by grazing scars, but by limpet choice.  To account for this concern, Haggerty and her colleagues chose 43 ungrazed kelp plants, placed three  limpets on one frond, and chose a second, equal-sized frond as an unmanipulated control. Once again, they visited their plants every three weeks, and discovered that grazed fronds broke first in all 20 pairs that the sequence of frond breakage could be determined.  Clearly, limpet grazing is bad news for feather boa kelp.

How does the señorita fit into this system? The researchers designed a laboratory experiment to address this question.  They used 10 large tanks (1700 L), and set up five different experimental treatments to compare direct effects of predation, and indirect effects of predator presence, on limpet grazing, and ultimately on kelp survival. To isolate the direct effects of predation from the indirect effects of predator cues on limpets, Haggerty and her colleagues placed four kelp fronds into fish exclosure cages, which were housed in the large tanks, and placed three limpets onto some of these fronds.  To mimic actual predation (CE treatment in Table below), they removed limpets by hand at a constant rate typical of señorita predation. For the NCE treatment (testing indirect effects of predator presence) they introduced señorita into the large tank so the limpets experienced the predator cues, but were not eaten. The different treatments are summarized in the table below. These experiments ran for one week and each treatment was replicated 10 times.

HaggertyTableFinalEach day the researchers monitored the number of limpets and grazing scars.  After one week, Haggerty and her colleagues counted the number of grazing scars, and measured the breaking strength of each frond by clamping the frond’s end to a table and pulling on the opposite end with a spring scale until it broke. They then recorded the amount of force needed to break the frond.


Clamped kelp frond whose breaking strength has been tested.  Notice that the frond broke at a grazing scar (right). Credit Miranda Haggerty.

Not surprisingly, the predator control (PC) kelp (limpets present without señorita) had the most scars and lost the greatest amount of tissue.  Kelp receiving the consumptive predator effect treatment (CE) had fewer scars and lost less tissue than PC.  But interestingly, kelp receiving NCE and TPE treatments had significantly fewer scars than the CE kelp, and were statistically indistinguishable from each other.  Thus, in the laboratory, the presence of señorita cues (NCE treatment) was more important than actual predation (CE treatment) in reducing kelp scarring and tissue consumption (top and middle graph below).  As a result, the NCE treated kelp were stronger (had greater breaking strength) than were the CE treated kelp (bottom graph below).


Mean (+ standard error) number of grazing scars (top), mass of tissue consumed (middle) and breaking strength (bottom) of kelp in response to five experimental treatments. CE = consumptive effect, NCE = non-consumptive effect, TPE = total predator effect, PC = predator control, LC = limpet control. Different letters above bars indicate significant differences between the means when comparing treatments.

Haggerty and her colleagues replicated this experiment, with a few experimental design modifications, in a field setting.  As with the laboratory experiment we’ve just discussed, the researchers found a very strong non-consumptive effect. The researchers suspect that these limpets respond to chemical cues emitted by their señorita predators. They could not respond to many types of sensory cues because they lack auditory organs, and the experimental design prevented fish from transmitting any shadows (visual cues) or vibrational cues. In addition previous studies have shown that some limpet species use chemoreception for predator avoidance, foraging and homing. However, the nature of this chemical cue is yet to be discovered for this predator-prey system.


Schooling señorita. Credit: Miranda Haggerty

Trophic cascades occur when the effects of one species on another species cascade down through the ecosystem. In this case, señorita predators directly and indirectly reduce limpet density, which increases the survival of kelp – a foundation species for this ecosystem. The researchers point out that this trophic cascade only occurs in the southern feather boa kelp range, because señorita are absent further north.  We don’t know if limpets have other predators in the northern range, but we do know that the kelp are structurally more robust further north, so they (and the ecosystem) may be relatively immune to limpet-induced destruction.

note: the paper that describes this research is from the journal Ecology. The reference is Haggerty, M. B., Anderson, T. W. and Long, J. D. (2018), Fish predators reduce kelp frond loss via a trait‐mediated trophic cascade. Ecology, 99: 1574-1583. doi:10.1002/ecy.2380. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Limpet larvae and their fantastic voyage

As he began his PhD program, Takuya Yahagi was puzzled by some laboratory findings. Juvenile red blood limpets, Shinkailepas myojinensis, seemed to survive and grow extraordinarily well at temperatures between 15-25° C. Adult limpets live in deep sea vent communities, where temperatures generally range between 6-11° C.

limpet photo

Adult Shinkailepas myojinensis.  These are approximately 6 mm in length. Credit: Takuya Yahagi.

Yahagi and his colleagues wondered why limpets are making babies that survive and grow at much higher temperatures than they are likely to experience after hatching.

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Deep sea hydrothermal vent community at 795 meters depth at Myojinsho Caldera in the northwest Pacific. White patches on the rocks are vast communities of chemosynthetic bacteria which are being grazed by purple/pinkish limpets. You can also see the white feathery feeding legs of a barnacle population in the upper portion of the photo. Credit: JAMSTEC

Yahagi reasoned that perhaps, in the natural world, the limpet juveniles live in different (warmer) environments than do their parents. If they migrated closer to the sea surface, their world would be somewhat warmer. But limpet babies are microscopic, so capturing them near the sea surface (and knowing that you had captured them!) is very challenging. Working with three other researchers, Yahagi decided to collect indirect evidence to test the hypothesis that baby limpets migrate to the surface where they feed and grow before returning to the ocean depths.


Larval S. myojinensis limpet 156 days after hatching. sh=shell, f =foot, e=eye, vl=velar lobe.

Initially, the researchers needed to determine what temperatures these growing limpets preferred. With the help of a remotely operated submarine, they collected adult limpets laden with egg capsules, and placed newly hatched larvae into separate containers under different conditions. Some larvae were fed and raised at one of six different temperatures: 5, 10, 15, 20, 25 and 30° C. Other larvae were starved at 5, 15 or 25° C to see how long they survived at different temperatures. If the larvae were migrating upwards to warmer waters, it was important to see how long they could survive until they arrived at the richer food sources near the surface.

Starved larvae survived up to 150 days at the lowest temperature, and for more than three weeks at 25° C, which provided ample time for upward migration (even at very mellow baby limpet swimming speeds). Fed larvae grew much more quickly at warmer temperatures, with best growth at 25° C, and no growth at 5-10° C, which is the approximate temperature at hydrothermal vents.. Larvae initially grew quickly at 30° C, but long term exposure to that temperature killed them.


Growth (shell length) of fed larvae at different temperatures.

These temperature profiles corresponded to temperatures at the sea surface down to about 100 meters, which ranged between 19-28° C. This correspondence supported the hypothesis that juveniles migrated upwards in the water column after hatching. But could Yahagi and his colleagues find any direct evidence for this vertical migration? To answer this question, they video-recorded new hatchlings in a clear plastic bath, and measured how fast these limpets swam, and what direction they preferred. They discovered that new hatchlings constantly swam upward in their test bath, and swimming speed was considerably faster at warmer temperatures.

The sea surface is a wonderful place to find food, because sunlight is abundant, so there are abundant phytoplankton to satisfy even the most voracious juvenile limpets. But sea surfaces also have very strong currents which can whisk juvenile limpets hundreds or thousands of kilometers away. The upshot is that vertical migration and wide dispersal of juveniles by ocean currents can introduce new genes into far-away limpet populations.

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A hot vent animal community at 700 meters depth at Minami-Ensei Knoll in the northwest Pacific. Prevalent groups include lobsters (white), two species of shrimp, mussels and two different limpet species. Credit: JAMSTEC.

Gene flow – the movement of genes from one population to another – has some important genetic impacts. Without gene flow, two populations that are separated from each other can become genetically distinct. But the mixing of genes from long-distance dispersal can prevent this from occurring. The researchers compared 1218 base pairs of the COI gene from 77 adult limpets that were collected from four different sites which were separated, in some cases, by more than 1000 kilometers. In support of the gene flow hypothesis they found no evidence of any genetic differentiation among the four populations.

Yahagi Fig1

Hydrothermal vent fields in the northwest Pacific Ocean.  Black squares are limpet collection sites for this study.  Notice the vast distances separating these populations.

Gene flow requires long distance dispersal, and the adult limpets travel very little along the sea floor. This finding of no genetic differentiation among the geographically separated populations supports the hypothesis that the juveniles migrate upwards, feed on abundant phytoplankton, and are carried to new distant environments. There, they mature and settle into new ocean vent communities where they can feed on the superabundant chemosynthetic bacteria associated with the ocean vents. But we still don’t know how limpets find a new ocean vent community – do they migrate, checking out possible vent habitats, while they are still juveniles and still capable of swimming? Do they have sense organs that pick up environmental cues such as hydrogen sulfide content, water temperature, turbulence or noise from vent emissions, to help them complete their fantastic ocean voyage?

note: the paper that describes this research is from the journal Ecology. The reference is Yahagi, Takuya, Hiromi Kayama Watanabe, Shigeaki Kojima, and Yasunori Kano. 2017. Do larvae from deep‐sea hydrothermal vents disperse in surface waters? Ecology 98: 1524-1534Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.