水研センター研報，第32号，95−102，平成22年
Bull. Fish. Res. Agen. No. 32, 95‑102, 2010

Inhibitory effects of wave action on destructive grazing
by sea urchins：a review
Shigeru KAWAMATA＊1

Abstract: Wave-induced water motion is one of the key determinant factors protecting kelp
assemblages from destructive grazing by sea urchins; however few studies have quantitatively evaluated the hydrodynamic effect on rocky subtidal community ecology due to thecomplex nature of the water motion. Our quantitative understanding of the effects of waves
on urchin foraging behavior has increased substantially over the past 15 years, primarily due
to flow tank experiments on the sea urchin, which have formed extensive urchin barrens in northern Japan. This review evaluates the mechanism and extent
that the oscillatory water flow influences the behaviors of sea urchins. The dislodgement
velocity for stationary sea urchins, which has been determined in various studies based on
the hydrodynamic theory, is discussed. Previously predicted dislodgement velocities for seaurchins are extremely high (> ca. 5 m/s) while the velocity limit for urchin movement ona smooth and flat substratum is much lower than 1 m/s. The importance of attachment by
spines to urchin movement in moving water is discussed. Dense cover of turf algae prevents
the effective attachment of the distal suckers of tube feet and thus substantially reduces
the critical velocity for urchin movement. Urchin climbing of upright thin objects, such as
anchor ropes of buoyed systems for kelp cultivation, to which little attention has been paid,
is discussed in relation to oscillatory water motion. Finally, the effect of oscillatory flow onurchin feeding is discussed.
Key words: barrens, grazing, kelp, sea urchin, waves

Introduction

Urchin barrens generally have low productivity(Mathieson1991) and are persistent.

Kelp beds have a fundamental role in maintaining

In northern Japan, sea urchins, such as

populations of various fish and invertebrates by

andalsoproviding food and habitats (Tegner and Dayton,

dominate significant areas of subtidal rocky bottom

2000; Edgarand have formed extensive urchin barrens, limiting

2004). Many kelp species are bothhighly productive (Mann, 1982) and have a highthe colonization of kelp (Nabatanutritive value for various herbivorous animals manyand Tada, 1994; Muraoka, 2008). These urchins areof which are of considerable economic importance, inlegally protected as fisheries resources exclusively

particular abalone and sea urchins (Uki, 1981; Ukifor the commercial fishing by the local fishermen s, 1986; Nabata

1992; Abe

1999; Scheibling and Anthony,cooperative. Nevertheless, few urchins are harvested

2001) However, sea urchins often are extremely

in barrens due to their poor growth and low quality

abundant and denude the substratum of erectof the edible gonad, allowing the maintenancemacroalgae, forming extensive

urchin barrens ,of urchin barrens. Many attempts including sea

and this phenomenon has been recorded worldwide

urchin removal and the placement of physical(Harrold and Pearse, 1987; Scheiblingbarriers (Kawamata, 2001a), have been made for, 1999).

2010年 月 日受理（Received on July 1. 2010）＊1
National Research Institute of Fisheries Engineering, Fisheries Research Agency
7620-7 Hasaki, Kamisu, Ibaraki 314-0408, JapanShigeru KAWAMATA
kelp restoration but most of them have failed, partlyof waves on urchin behavior has increased

because of the high mobility of sea urchins.

substantially over the past 15 years, primarily due

The wave-induced oscillatory water motion, whichto flow-tank studies. I have used two different flow

increases with decreasing depth, is one of the mosttanks for urchin-behavioral studies. The first an

important factors controlling urchin grazing. Sea

oscillating flow tank, which is a U-shaped pipe withurchins undoubtedly have the ability to move ona piston, reproducing wave-induced oscillatory flows.

any type of substrata, including rock overhangs,

In addition, a circuit flume tank which can reproduce

rugged mussel beds, algal turf areas, plastic netting

standing waves with a reversible impeller. In thisfences and upright thin ropes, by maneuvering theirreview, I discuss the hydrodynamic effects on urchintube feet and spines. However, sea urchins are rare

behaviors in relation to attachment, movement andin wave-exposed shallow areas, allowing macroalgae

feeding.

to survive and grow, with the presence of abundanturchins in the adjacent barrens. Such a distributionalAttachment

pattern of kelp beds and urchin barrens is common
in the temperate zone. In rocky subtidal areas on theThe ability of a benthic organism to withstandnortheastern Pacific coast of Honshu, the main islandstrong water motion depends on its attachmentof Japan, the sea urchinstrength relative to the hydrodynamic forces. Sea

forms extensive and persistent urchin barrens, buturchins apparently achieve greatest attachment

wave-exposed shallow reefs are generally dominatedstrength by the use of both their spines and tube

by kelp such as

Although manyfeet for bracing and adhesion in shelter holes orecologists have described the importance of wave

crevices. During foraging outside of shelters, theaction in the rocky subtidal community structure,use of spines in bracing is necessarily reduced,

few studies have quantitatively assessed it, partly

thus making the tube feet the primary mechanism

because wave-induced water motion is highlyof attachment (Lissner, 1983; Kawamata, 1998).

variable over time and complex. In principle,

A stationary organism in unsteady, oscillatory

however, wave-induced water motion can bewater motion experiences the acceleration force

measured and predicted by engineering techniques,in addition to the forces (i.e., drag and lift) caused

and thus quantitative assessment will provide usefulby instantaneous water velocity (Denny, 1988). At

insights into not only the spatial distributions ofintertidal sites, the acceleration force imposed onurchins and algae but also practical methods for kelpa stationary organism is significant because therestoration.

water acceleration can be extremely high, overOur quantitative understanding of the effects

100 m s‑2 (Denny, 1985; Gaylord, 1999). At subtidal

Table 1. Dislodgement velocity for sea urchins

1)

Prediction at which 50% urchins will be dislodged.
Prediction for the maximum attachment force which an urchin should achieve by attachingwith all their adoral tube feet.
3)
Prediction for attachment forces measured in the field.
2)Inhibitory effects of wave action on destructive grazing by sea urchins：a review
sites, however, the acceleration force is virtually

decreasing depth but is limited due to the wave

negligible, because when wave-induced orbital

breaking. Although the ratio of the wave height

velocity reaches a maximum, water acceleration

to depth at breaking varies in a complex relation

becomes zero, and because the wave-induced waterwith the bottom slope and the steepness of waves,acceleration is much lower than the gravitational
acceleration of 9.81 m s‑2 (Barber, 1969; Kawamata,2001b). Thus, an estimate of the dislodgement
velocity, defined as the critical velocity at which
an organism will be dislodged, is obtained as thevelocity at which the velocity-induced force becomesequal to the attachment strength. Dislodgement
velocities predicted in this manner for urchin species
are summarized in Table 1.
The wave-induced water velocity in subtidal areas
is limited by water depth. The maximum watervelocity,, caused by waves in shallow water ismaxmax

where2m s ),

= 0.3

(+ )

(1)

is the acceleration due to gravity (= 9.81
the wave height, andthe water depth(Denny, 1988). The wave height increases withFig. 1. Maximum rate of movement ofin oscillatory flow
(Kawamata, 1998).

Fig. 2. Intrusion ratios offor the control flat plate andexperimental substrata in different velocity amplitudes (Kawamata and Furuhata,
unpublished data). Error bars indicate 95 % confidence intervals.

Shigeru KAWAMATA
possible ratios are limited to as high as 1.4 for steep

represents the intrusion ratio, defined as the ratio ofslopes (Denny, 1988). Thus, the maximum possible

the number of the intrusion successes (mountingwater velocity isa test substratum entirely) to that of the intrusion

max= 0.46trials(2)(contact with the edge of the substratum).

The intrusion ratio remained as high for the stick

It is predicted from Eq. 2 that the dislodgement

bed and for the artificial turf as for the control flat

velocity of sea urchins is very unlikely to occur inplate at a velocity amplitude of 0.35 m/s. In contrast,subtidal areas. For example, whenmax

the ratio was significantly lower for toweling thanis only 2.9 m/s. Taking into account the additional

for the stick bed even at as low as 0.15 m/s. The

attachment strength due to bracing of spines, themechanism for toweling to inhibit urchin invasion

distributional area of sea urchins generally cannot

is very simple. Tube feet attach to the substratum

be limited by the wave-induced dislodgement whilewith their distal suckers. On toweling, however, thebeing stationary.

suckers fail to achieve an effective attachment to the= 4 m,

fabric texture of the toweling, so that urchins cannot
Benthic movement

easily move in moving water.
A good example of such substratum effect inDuring movement, urchins are much morenature is the colonization of barren substratum

subject to the effects of water motion than whenby rapid-growing turf algae prior to the formation

attached while being stationary. Fig. 1 shows theof kelp

maximum rate of movement by

Japan coast of Hokkaido, northern Japan. The kelp

stands on the Sea of, which was stimulated with a spot light ingenerally dominates the wave-exposed shallow

oscillatory flows. The urchins showed minimal

area from mid winter to early summer, while after

ability to move at about 0.7 m/s. Attachment tosummer

the substratum by tube feet is a primary factor

substratum of erect macroalgae up to the upper

affecting the mobility of sea urchins. This was foundlimit of the subtidal area forming extensive barrens.

by the oscillating-flow-tank experiment (KawamataIn the absence of non-crustose algae, sea urchinsand Furuhata, unpublished data) which tested theforage even to the uppermost part of the subtidal

inhibitory effects on sea urchin invasion over several

zone exposed to surging waves (Fig. 3A). When an

types of substrata, including a stick bed, artificial

algal carpet is formed, however, then sea urchins are

turf and toweling (Fig. 2A, B and C). Contrary to

excluded from the area, even at calm sea conditions

initial speculation, only toweling had a clear effect(Fig. 3B).

denude theon urchin invasion, as shown in Fig. 2. The ordinate

Fig. 3. The uppermost part of the subtidal on the Sea of Japan coast of Hokkaido immediately before (A; 27December 1999) and after early colonization of algae (B; 4 January 2000) (Kawamata, 2001a).

Inhibitory effects of wave action on destructive grazing by sea urchins：a review
Vertical movementon the climbing performance offor

swingable and fixed columns covered by microalgae
Little was known about vertical movement inin oscillatory flow (Fig. 5). Contrary to initial

sea urchins, and line cultivation methods have been

speculation, sea urchins also climbed the swaying

used in urchin barrens without much consideration

upright objects if food was un available elsewhere.

for the climbing ability of sea urchins. Actually,
Feeding

however, sea urchins climb even thin vertical ropes
as long as food is limited on the seabed (Fig. 4). A
recent laboratory study (Kawamata, 2008) showed
the high climbing performance ofFeeding is even more susceptible to water motion
than movement because the mechanical instability

in oscillatory flows using upright rods of 10of sea urchins increases during feeding as follows.

and 3 mm diameters with algal food items attachedSea urchins have their mouth at the center of theirat 2.5 cm intervals. In this case, sea urchins climbed

attachment base so that they must detach more

the rods to graze on food items from the bottom

than half the number of their tube feet used to cling

one by one although they did not always reach theto the substratum while feeding. At the same time,

top food item. In the absence of oscillatory flows,

the animals must overcome the additional dragurchins readily climbed and grazed on almost all theon algae. Therefore, the upper velocity limit forfood items even for thin rods. Urchin climbing was

feeding on foliose macroalgae is lower than that for

reduced in height and in frequency as the velocity

movement (Kawamata, 1998). Oscillating-flow-tankamplitude increased. However, the animals werestudies (Kawamata, 1998; 2001a) indicated that theable to climb even at 0.4 m/s regardless of the rod

velocity limit for feeding may somewhat vary withdiameter.

animal size and algal morphology but is limited toA flume tank experiment was also conductedless than ca. 0.4 m/s.

Fig. 4. Sea urchins () climbing anchor ropes to feed on algae in an urchinbarren of Miyagi, Prefecture northeastern Pacific coast of Honshu.

Shigeru KAWAMATA

Fig. 5. Sea urchins () climbing on swingable as well as fixed rods in theoscillatory flow with the velocity amplitude of 0.15 m/s (Kawamata unpublished data). The microalgae
had initially covered the entire surface of both kinds of rods (A) and then were almost completely
grazed by climbing urchins on day 5 (B).

Fig. 6. A flume tank experiment on the foraging behavior of the sea urchinin the vicinity of abed placed on the top of a mound (Kawamata, 2001a).

In addition, the wave-induced movement ofmacroalgal fronds, called thewhiplash

bed placed on the mound under waves

effect,(Fig. 6). In the experiment, strong and weak wave

may repel urchins away from macroalgal stands.

periods were repeated over a 12 day period in theAlthough many studies described the importancepattern shown in Fig. 6. The velocity amplitude atof the whiplash effect in the survival of algal

the top of the mound where kelp plants were placed

stands in dense urchin barrens (e.g. Velimirov andwas higher than that at the bottom of the mound.

Griffiths, 1979; Himmelman, 1984; Dayton, 1985;

The movement of the urchins up and down theKonar, 2000; Gagnon

2003; Konar and Estes,slope in response to the change in water velocity

2003), few studies have quantitatively assessed

was clear from the results aggregated at the edge of

the water motion which cause the movement of

the kelp stands as the water motion decreased. On

algal fronds (Kawamata, 1998; 2001a; Gagnon

the contrary, they began to move back away from2006). Kawamata (2001a) conducted a flume tankthe stands when the velocity amplitude increased

experiment on the behaviors ofbeyond only 0.1 m/s.

around aInhibitory effects of wave action on destructive grazing by sea urchins：a review
Conclusionof(Phaeophyta).
, 334, 10‑19.

Foraging activity of sea urchins is greatly

Gaylord B., 1999: Detailing agents of physicalaffected by wave action through limiting movement

disturbance: wave-induced velocities andand feeding rather than through dislodgement.

accelerations on a rocky shore.

The effects of waves on urchin behaviors can239, 85‑124.

be quantitatively understood by laboratory
flow-tank experiments, while wave-induced water

Harrold C. and Pearse J. S., 1987: The ecological roleof echinoderms in kelp forests.

motion is too complex to readily assess in nature.
Such quantitative information coupled with theM. Jangoux and J. M. Lawrence, Eds.,
A.A.Balkema, 137-233.

assessment of water motion will provide insights not

Himmelman J. H., 1984: Urchin feeding andonly into urchin-kelp interactions but also into usefulmacroalgal distribution in Newfoundland,

methods for kelp restoration in urchin barrens.

111, 337‑348.

eastern Canada.

Kawamata S., 1998: Effect of wave-inducedReferences

oscillatory flow on grazing by a subtidal seaurchin(A-Agassiz).
, 224, 31‑48.

Abe E. and Tada M., 1994: The ecology of asea urchin,

Kawamata S., 2001a: Effect of waves on grazing(A. Agassiz) on the coast of Okhotsk sea inby sea urchins and abalone on the coast ofHokkaido.

northern Japan.

45, 45‑56 (in Japanese).

1, 59‑107(in Japanese).

Barber N. F., 1969:

Wykeham.

Kawamata S., 2001b: Adaptive mechanical tolerance

Dayton P. K., 1985: Ecology of kelp communities.

and dislodgement velocity of the kelp

16, 215‑245.

in wave-induced water motion.
211, 89‑104.

Denny M. and Gaylord B., 1996: Why the urchin lostits spines: hydrodynamic forces and survivorship
199, 717‑729.

in three echinoids.

urchinDenny M. W., 1985: Wave forces on intertidal
30,

organisms: A case study.

Kawamata S., 2008: Climbing performance of sea

1171‑1187.

for upright, thinobjects in wave-induced oscillatory flow.
74, 1005‑1016.
Konar B., 2000: Seasonal inhibitory effects of marine

Denny M. W., 1988:

plants on sea urchins: structuring communities
Princeton UniversityPress.

the algal way.

, 125, 208‑217.

Konar B. and Estes J. A., 2003: The stability ofEdgar G. J., Barrett N. S., Morton A. J., and Samson
C. R., 2004: Effects of algal canopy clearance onplant, fish and macroinvertebrate communities
on eastern Tasmanian reefs.
312, 67‑87.
Gagnon P., Himmelman J. H., and Johnson L. E., 2003:
Algal colonization in urchin barrens: defense

boundary regions between kelp beds anddeforested areas.

Lissner A. L., 1983: Relationship of water motion tothe shallow water distribution and morphology
41,of two species of sea urchins.
691‑709.
Mann K. H., 1982:

by association during recruitment of the brown
alga

84, 174‑185.

Blackwell, 322 pp.
Mathieson A. C., Penniman C. A., and Harris L. G.,

290, 179‑196.

1991: Northwest Atlantic rocky shore ecology.

Gagnon P., St-Hilaire-Gravel L. V., Himmelman J. H.,

A. C.

and Johnson L. E., 2006: Organismal defenses

Mathieson and P. H. Nienhuis, Eds., Elsevier,versus environmentally mediated protection

109‑191.

from herbivores: Unraveling the puzzling case

Muraoka D., 2008:

bed coverageShigeru KAWAMATA
off Oshika Peninsula, Japan, in relation tosporophyte survival and20, 845‑851.

abundance.

Nabata S., Abe E., and Kakiuchi M., 1992: On theIsoyake condition in Taisei-cho, southwestern
Hokkaido.
38, 1‑14 (in Japanese).
Nabata S., Hoshikawa H., Sakai Y., Funaoka T.,
Oohori T., and Imamura T., 1999: Food valueof several algae for growth of the sea urchin,54, 33‑40 (in Japanese).
Santos R. and Flammang P., 2007: Intra- andinterspecific variation of attachment strength in332, 129‑142.

sea urchins.

Scheibling R. E. and Anthony S. X., 2001: Feeding,growth and reproduction of sea urchins() on single andmixed diets of kelp (spp.) and theinvasive algassp.

139, 139‑146.
Scheibling R. E., Hennigar A. W., and Balch T., 1999:
Destructive grazing, epiphytism, and disease:the dynamics of sea urchin − kelp interactions
56,in Nova Scotia.
2300‑2314.

Siddon C. E. and Witman J. D., 2003: Influence ofchronic, low-level hydrodynamic forces onsubtidal community structure.
261, 99‑110.
Tegner M. J. and Dayton P. K., 2000: Ecosystemeffects of fishing in kelp forest communities.
57, 579‑589.
Uki N., 1981: Food value of marine algae of order
Laminariales for growth of the abalone,42, 19‑29.
Uki N., Sugiura M., and Watanabe T., 1986: Dietary
value of seaweeds occurring on the Pacific coastof Tohoku for growth of the abalone, 52,257‑266.
Velimirov B. and Griffiths C. L., 1979: Wave-induced
kelp movement and its importance forcommunity structure.

22, 169‑172.