sea urchin (strongylocentrotus droebachiensis) aggregating behavior investigated by … ·...

Sea Urchin (Strongykocenh.otus droebachiensis) Aggregating Behavior Investigated by a Subtidal Multifactorial Experiment

Richard W. Wejsford Research Group Limited, Suite 6 , 2nd Floor, Collins Court, Historic Properties, 4869 Upper Water Streat, Halifm, N.S. B3J IS9

Department of Bio&ogy, Univcr.&y of Southern Cabdfornis, Lss Angeles, CA 90009, USA

Marine Ecology Laboratory, Bedford Institute of Oceanography , B.O. Box 6006, Dartmouth, N.S. B2 Y 4A2

BEBNSTEIN, 8. B., S. C. SCHWOETEW, .4ND K. M. N%EPNN. 1983. Sea urchin (Strongylocen- trotus droebachiensis) aggregating behavior investigated by a subtidal rnultifacto- rial experiment. Can. J. Fish. Aquat. Sci. 40: 1975- 1986.

We performed a multilevel factorial field experiment tea identify the effects of five factors on sea urchins' (Strongylocentrstus drsebachiensis) aggregating behavior. The factors were ( I ) source of urchins (kelpbed or barrens), (2) density sf urchins (high or low), (3) location sf treatment (kelpbed or barpens), (4) the presence and type of invertebrate predators (crabs or lobsters), and (5) season (summer or winter). These manipulative experiments were performed in flexible, resilient cages designed to withstand the severe wave surge in Nova Scotia's shallow subtidal environment. Interactions identified by ANBVA among the various factors showed that urchins aggregate meare at high (20.m1=) than at low (49rn-') density. The presence of lobsters in the kelpbed, and sf crabs in the barrens. triggered the formation of even larger aggregations. These aggregations remain in the open even in the presence of predators. We argue that this behavioral mechanism (a defensive aggregation response to lobsters in the kelpbed) is the trigger that precipitates widespread destructive urchin grazing and the transformation of kelpbeds to barrens. Lobsters thus play two opposite roles. At low urchin density lobsters keep urchins in hiding and thereby contribute to kelpbed persistence. At higher urchin density, lobsters trigger the formation of Iarge, exposed urchin aggregations that graze destructively on kelp. Urchin responses to predators are probably mediated by a combination of conditioning and sensitivity to biochemical cues. The large-scale change in community structure, from kelpbed to barrens, can thus be understood in terms of the adaptive behavioral responses of individual organisms. We review the roles of other predators in this system and show that they have varying effects on the intensity of urchin grazing, depending on urchin density, season, and habitat type.

BERNSTEIN, B. B., %. C. SCHROETER, AND K . H. MANN. 1983. Sea urchin (Strongylscen- trotus droebachkensds) aggregating behavior investigated by a subtidal multifactorial experiment. Can. J. Fish. Aquat. Sci. 40: 1975- 1986.

Nous avons men6 sur le terrain une exp6rience rnultifiactorielle en vue d'identifier les effets de cinq facteurs sur le comportement d'association de I'oursin de mer commun (Stron- gybocentrotus droehaechiensis). Les facteurs CtudiCs ont CtC (1) la source des oursins (lit de varechs su fond denude), (2) la densit6 des oursins (ClevCe ou faible), (3) 19endroit du traiternent (lit de varech su fond dCnudC), (4) la prisence et Be type de prChteurs invertCbr6s (crabes ou homards) et (5) la saison (kt6 s u hiver). Ces manipulations ont CtC effectukes dans des cages rksilientes flexibles, consues pour risistqr au dkferlement des lames dans l'en- vironnement subtidal peu profond de la Nsuvelle-Ecosse. Les interactions identifiees par ANBVA entre les divers facteurs dkmontrent que les oursins se rassemblent davantage ii une densite Clevke (20.m-') qu'a une densite faible (4-mp2). Les associations sont encore plus fortes en prCsence de homards sur les lits de varechs et de crabes sur %es fonds denudes. Ces associations demeurent a dkcouvert m2me en presence de prkdatemrs. Nous arguons que ce mCcanisme Cthologique (rkponse defensive d'association en presence de h a r n ~ d s sur le lit de

Printed in Canada (J7284) Imprime au Canada (J7284)

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CAN. J . FISH. AQUAT. SCI., VOL. 40. 1983

varechs) cst le facteur qui dkclenche le broutage destructeur chez les oursiras et la trans- :ormation des lits de varechs en fonds dknudks. Les homards jouent donc deux rciles opposis. A une faible densite d'oursin:, ils fsrcent ces derniers B se cacher, contribuant ainsi au maintien des lits de varechs. A une densite plus ClevCe d'oursins, les homards dtclenchent la formation d'impsrtantes associations d90ursins exposCs yui broutent les varechs jusqu'i les dCtruire. Ees oursins reagissent en presence de predateurs probablernent par l'intermkdiaire d'une combinaison de conditionnement et de sensibilitk il des indices biochimiqucs. De grands changernents de structure de la comrnunautC, ssit d'un lit de varechs il un fond dCnudC, p u t donc s'expliquer en terme de reaction dthologique adaptive d'organismes individuels. Nous examinsns le rdle des aukres predateurs dans ce systhme et dCmontrons qu9ils produisent des efets varies sur I'intensitk du broutage par les oursins, selon la densit6 de ces derniers, la saison et le type d9habitat.

Received March '7, 1983 Accepted July 27. 1983

MLICH evidence points to the large-scale disappearance of algal beds from coastal Nova Scotia, Canada, and their replacement by sea urchin dominated banen grounds between about 1960 and 1980 (Breen and Mann 1976; Mann 1977; Whabl-ton and Mann 1981). Field observations have established that urchins, feeding in dense aggregations, are the proximate cause of the shift from kelpbeds to barrens. The formation of these aggregations, which represents a change in urchin foraging behavior, is thus the trigger point that precipitates the radical change in system state. We have shown (Bernstein et al. 1981) that urchin (Strongjlocevftrotus droe- bnchkensks) aggregating behavior is flexible. Urchins, even at relatively high densities, hide during the summer when large predatory fish are present and forage only at night when the fish are inactive. The presence of crabs caused urchins in the laboratory to aggregate in the open as a defensive clumping response. This led us to hypothesize that a defensive clumping response to invertebrate predators in the kelpbed (crabs or lobsters) could trigger the formation of destructive grazing aggregations, once urchin density had passed a critical thresh- sSd.

This is intriguing because it implies that predation, even in this relatively simple system, can be either stabilizing or destabilizing, depending on the type of predator and urchin defisity. In addition, a behavioral rather than a numerical change in the response of a mobile and behaviorally flexible prey to a single predator may provoke a large-scale shift in ecosystem state. This provides the possibility for understanding in detail the mechanisms that link the behavior of individual organisms to large-scale features of community structure. The Geld experiments we describe below were undertaken in an attempt to identify the operation of the behavioral trigger point in aggregation formation. We wished to test the hypothesis that aggregating behavior is intensified by defensive responses to certain predators. In addition, we wanted to determine the ways in which major environmental features such as season and habitat (kelpbed or banen) inter- acted to set limits to urchins' aggregating behavior.

Study Site

We performed the experiments at 8 to 10 m of depth at Green Island, near Cape Sable on the exposed southwest coast of Nova Scotia. This site included healthy Lanainaria beds

R e p Be 7 mars 1983 Accept6 16 27 juillet 8983

and established barrens in close proximity, as well as popu- lations of urchins at densities characteristic of these two hak- itats. In the kelp area, the substrate consisted of Barge granite boulders, the largest being several metres in diameter. Algal cover approached 90% and consisted primarily of Laminaria iovfgicruris and L. digltata with an understory of Chondrefs crispus. Desrnarestia viridis was seasonally abundant in the summer. Nova Scotia9s nearshore subtidal kelpbeds are described in greater detail in Mann (1972). Urchin densities in the kelp were low (<5.m-'); all individuals were large (>35 mm) and hidden In crevices in both winter and summer. This area was exposed to severe winter storms from the west and northwest. Gales lasting for several days, with wind velocities in excess of 76) km-h-band swells to 7 m were common during the winter experiments.

The banen area was slightly less exposed. The substrate was granite boulders (to I rn diameter) with occasional patches of coarse sand. There was scattered Agarurn crikro- $urn but no Laminaria or ChoneZyus. Urchin densities were higher than in the kelp area (20-30. m -') and these were predominantly exposed rather than hidden. Water temperatures at both sites ranged from 1°C in the winter to 12°C in the summer.

Materials and Methods

The Geld experiments were designed to detect the effects of five factors on sea urchins' aggregating behavior. These factors were (1) source of urchins (kelpbed or barrens), (2) density of urchins (high or low), (3) location of treatment (kelpbed or barrens), (4) the presence and type of invertebrate predators (crabs or lobsters), and ( 5 ) season (summer or winter).

Our previous work had indicated the importance of each of these factors in aggregating behavior. Urchins from the barrens are starved relative to kelpbed urchins. This difference in nutritional state affects their movernent patterns (Bernstein et al. 1981; Mattison et al. 1977) and n~ost probably their response to biochemical cues. Clumping is more prevalent at high urchin densities (Bernstein et al. 198 1). The kelpbed and the barrens differ in the amount and type of food and shelter and harbor distinct suites of predators. Finally. both inver-

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BERNSTEIN ET AL.: SEA URCHIN AGGREGATING BEHAVlOR

TABLE I . Factorial experimental design. Urchins from kelpbed and barrens were transplanted to cages in the kelpbed and in the barrens, at both high and Iow densities. and in the presence and absence of predators. All treatments were performed in winter and summer.

Source Habitat of Density Replicates

Season of urchins experiment of urchins hedators Winter Sumn~er

Crabs Lobsters None

High

Kelpbed

Low Crabs Lobsters None

Crabs Lobsters None

High

Barrens Crabs Lobsters None

Winter 4- summer

Crabs Lobsters None

High

Crabs Lobsters None

Low


High

Barrens


tebrate predators and season of the year affect urchins' clumping and foraging behaviors. We designed the treatments as a five-way factorial experiment with replication (Table 1). We coBBected large sea urchins from kelpbed and barrens habitats and transplanted them to cages in the kelpbed and in the banens, at high or low urchin densities, and in the presence and absence of invertebrate predators.

We utilized the factorial design because of its power and efficiency (Snedecor and Cochran 1967; Underwood 198 1) and because we were specifically interested in interactions among the factors. All factors were fixed effects, and the experiment was thus a model I analysis of variance (ANOVA), with all significance tests performed with the replicate or residual emor in the denominator sf the F-test. The level of replication was determined in part by logistical constraints. We did, however, perform pilot experiments that demonstrated that three replicates provided sufficient power to detect the predicted changes in clumping behavior.

Successful mmipulatians required the design of cages that could withstand the severe environmental conditions without interfering with urchin behavior. This task was complicated by the hardness of the granite substrate, which made drilling holes far cage supports unfeasible, and the extremely cold water temperatures, which prevented the use of marine

epoxies. We developed flexible, circular cages made of 5.6-cm monofiiament mesh stretched over plastic hoops and anchored by guy ropes to a grid of chains (Fig. I). This design was very transparent to wave surge and was quite resilient so long as the guy ropes were reglalady inspected and main- tained. All the cages survived several 3-d gales, and half of them survived m 8-68 storm.

We deployed 36 cages, 18 in each habitat. All were 1.2 m in diameter, covering an area of 1.0 mZ. This was large enough to ensure a variety of cryptic and exposed habitats in each cage. We avoided placing the cages on open sand patches or the flat faces of huge boulders and placed them in habitats with the same mix of substrates. The cage walls acted as additional structure, and urchins responded to them as they did to natural ledges and crevices (see Discussion for an analysis of possible cage effects). Urchin escape rates were extremely Isw (C10%), but about one third sf the lobsters and crabs escaped in the summer when these crustaceans were most active; all such experiments were discounted and repeated immediately.

Each replicate treatment ram for 3-6 d, depending on the weather. Low- and high-density treatments contained 4 and 20 urchins, respectively. This low density (4*m--') is wear the upper range of urchin densities in healthy, persistent

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CAN. J . FBSH. AQUAT. X I . , VOL. 40, 1983

FLOAT

OPENING Wl DRAWSTRIM

AIR-FILLED POLYETHYLENE HOOP

2.5 INCH MONOFIUlM€ MESH NETTING

POLYETKYLEME H O W

/ CHAIN WEffiHTp WITH CHAIN

FIG. I . (A) Cage system. Guy ropes were fastened to a grid of chains anchored to large boulders. Small buoys kept the cages erect, but allowed them to flex in response to surge. Each cage was 1.2 m in diameter and 1 m high. (B) Details sf an individual cage.

Laminaria beds. The high density (28- rapp2) is below that at which urchins are found in exposed feeding fronts (80.m-') (Bermstein et al. 1981). We selected 20-1n-~ because we wished to observe urchin behavior at the threshold of clump formation. Field observations of urchin grazing in St. Margaret's Bay and pilot experiments suggested that this occurred at about 20- 30 urchins - m12. Predator treatments contained one lobster or two crabs, with their claws banded. All animals were used for one replicate only and were then discarded. Urchins and crabs were captured locally; lobsters were either captured locally or purchased from fishemen immediately after capture.

Data were collected by scuba divers who inspected each cage and recorded their observations by mapping the location of each urchin and predator. They noted whether each urchin was hidden or exposed (as in Bemstein et al. 1981) and the size and location of all clumps sf two or more urchins. Wep- licates were discarded if more than 25% of the urchins could not be located or if the predators had escaped.

We calculated the following variables for each replicate treatment: mean clump size, percent sf urchins clumped, and percent of urchins in contact with the cage wall. These were calculated separately for all urchins in the cage, urchins in the

open, and urchins in hiding. In addition, we calculated the percent of urchins in each cage in hiding.

As in Bemstein et al. (B981), we defined a clump as any group of two or more urchins in contact. We calculated mean clump size by dividing the total number of urchins by the number of separate urchins or groups of urchins in the cage. Thus, a cage in which four urchins were distributed as a group sf two and two separate individuals would have mean clump size or 4/3 or 1.33. Clump sizes of 8 occurred oceasionally. If all the urchins in a cage were in hiding, for example, then the mean clump size of urchins in the open was defined as 0. Clump size in hiding was calculated on the same basis as urchins in the example above.

We analyzed each variable separately with ANOVA (fixed effects, general linear model, unbalanced design). We chose to analyze each variable for the total population of urchins and again for those podons of the population in open and cryptic subhabitats. We did this, despite the slight redundancy , because our previous work (Bemstein et a%. B 98 I) showed that urchins in these subhabitats sometimes behave differently. This approach also enabled us to determine which component of the urchin population was contributing most sf the overall Rsponse.

Percentage values were transformed prior to analysis with the m sine square root transformation. Mean clump size values were transformed to Boglo (x + I) to counter effects of

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BERNSTEM ET AL.: SEA URCHIN AGGREGATING BEHAVIOR

TABLE 2. Means of the replicates of each experimental treatment outlined in Table 1 . A11 variables calculated for each treatment are shown. Two or more urchins in contact were considered a clump. "Total" variables were calculated using a%! urchins in each cage, while "open" and "'cryptic" variables were calculated only from urchins in these subhabitats.

Source Habitat of Density Mean clump size

8 clumped % on wall of

urchins experiment of urchins Predators 9% cryptic Total Open Cryptic Total Open Cryptic Total Open Cryptic - p p p p p

( a ) Means for winter experrMen~s

Crabs Lobsters None

High

Kelpbed

Low Crabs Lobsters Nom

Crabs Lobsters None

High

Barrens


Cwbs Lobsters NOPI&

High

Kelpbed



High


I . 16.7 0.0 33.3 1.5 50.0 0.0 67.8 1.5 25.0 0.0 50.0

( b ) Means for summer experiments

Low

Crabs Lobsters None

High

Crabs Lobsters None

Low

Crabs Lobsters None

High

Crabs Lobsters None

Crabs Lobsters None

High

Crabs Lobsters None

Low

Crabs Lobsters None

High

Barrens


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1980 CAN. J . FISH. AQUAT. SCB., VOL. 40. 8383

nonnornmality. An examination of the variances showed that they did not exceed the limits of robustness of the F-test described by Green (1999) and Harris (1975).

We examined significant interactions with interaction plots that displayed the lat ti on ships among factors. The 0.05 Icvel was used for all significance tests with the F-test.

The interpretation sf higher ordcr interactions in a nmulti- level factorial design can be difficult unless it is based on explicit predictions, s r unless it is possible to assign clear biological meaning to them. Fortunately, we have been able to do both (see Results). We gave relatively less attention to effects that, while significant, were smaller or weaker. We found this design, even though complex. invaluable for two reasons. First9 our previous studies demonstrated that several factors act together to influence aggregating behavior. The only way to identify how these factors interact in nature is with a factorial experiment. Second, the factorial design provides the most statistically and logistically efficient means of testing for the effects of several hctors, either in isc~lation (main effects) or in combination (interaction effects).

Table 2 presents treatment means for the winter and summer sets of experiments. Table 3 siumnnarizes results of ANOVA by indicating, for each variable, which main effects and interactions were significant. As suggested by SokaI and Rohlf (1 969) and Snedecor and Cochran ( 1967), we discussed in detail only the highest level interactions involving each factor. This is because a sitnple statement about the effects of one factor is ambiguous when the effect is modified by the action of a second or third factor. For example, it would be inaccurate to say only that clump sizes are larger at high urchin densities, when the size of the effect depends on whether the experiments take place in the kelp or in the barrens and on whether or not a lobster is present. Table 3 displays ai~alyses of variance for these higher level interactions. Table 4 shows means for strongly significant main effects.

Two variables were measures of clumping behavior: the percentage clumped and the mean slump size. The prceartage clumped is somewhat, but not completely, correlated with mean clump size. This is because clump size can increase from 1.0 (when no urchins are clumped) only if thc percentage clunaped increases. Once some of the urchins are clumped, however, it is pss ible for mean clump size to increase when those urchins rearrange themselves into fewer, but larger, groups, without changing the percentage clu~npcd. These variables measure slightly different aspects s f clumping behavior. Mean clump size is naore sensitive to the intensity of aggregation, i.e. the degree to which urchins form large clumps.

The influence of urchin density on both clump size and percentage clumped was conspicuous (Table 4). In general, urchins clump more at high densities, although this effect is modified by the action of other factors. The density effect on clump size is partly a reflection of the higher upper limit on

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BERNSTEIN ET AL.: SEA URCHIN AGGREGATING BEHAVIOR 1981

TABLE 4 Strongly significant main effects. An asterisk indicates that the factor was nor inciuded in any higher order Interacttons. The other main effects, particularly density. were strong enough that their influence was apparent even in significant higher carder interactions.

Mean clunlp size 5% clurnpeci % ow wall Source of variation % cryptic Total Open Cryptic Total Open Cryptic Total Open Cryptic

Season Winter 2 9 J Summer 43.4

Source Kelp 53.2* 4 5 . F Barrens 45.2 43.0

Habitat Kelp 40.9 37.0" Barrens 57.8 54.2

Density High 1.9 l . $ * 2.0* 54.9 49.6 48.7 Low 1.2 1.0 0.9 19.8 13.7 12.8

Treatment None Crabs Lobsters

potential clump sizes in the high-density treatments. Several significant interactions (Table 3; Figs. 2-4)

describe the ways in which the other four factors combine with each other, and with density, to influence clumping behavior. The most important of these is the habitat X density x predators interaction (Fig. 2), which affects both mean clump size and percentage clumped. This demonstrates that at high urchin density, the presence of lobster$ increases clumping in the kelpbed, and the presence sf crabs increases clumping in the barrens. These predator effects are notable in two respects. First, they are nauch more marked at high than at low urchin density, unlike most of the other interactions discussed below. Second, the magnitude of the effect of predators on clump sizes is comparable with that of the very strong and pervasive effect of density. The mean clump sizes sf 2.2 (high urchin density in the banens, with crabs) and 2.3 (high urchin density in the kelp, with lobsters) are the largest encountered in any of the statistically significant interactions. Whereas seasonal effects were not statistically sip- nificant, mean clump sizes in the high urchin density lobster treatments In the kelp during the winter were higher yet (i.e. 2.9) (Table 2a).

These differences In clump size may seem small Be.g . 1.8 to 2.3 s r 2.9), but they represent an important change in the dispersion patterns of urchins in the cages. Clump sizes of around 1.8 typically result from three or four clumps of three or four urchins each iam a cage with 20 urchins. Clump sizes much above 2.8. however, always include one clump of at least 8 - 10 urchins (Table 5). This change in clumping pattern is significant kcause a clump of 10 grazing urchins is large enough to hold down and cause severe damage to Laminaria plants. while a clump of three or four urchins is much less able to do so. In the spring of 19'98, we observed the fomation of a localized urchin feeding aggregation along the edge of a kelpbed in St. Margaret's Bay (Bernsteina et al. 1981). As urchin density increased above 20. m -< groups of two to four urchins appeared, clustered aro~md Laaninaria holdfasts and stipes. There were occasional clumps sf 10 or more urchins

holding down entire Larnirzaria plants. As urchin density con- tinued to increase, these large clumps became Inore frequent and gradually merged to f s m a solid mass as urchin density approached 100 - rn '.

We believe these high-density treatments in the kelp with lobsters demonstrate the initial fomation of destructive feeding aggregations. Thc fomation of these aggregatisams depends on high urchin density, the presence of kelp, and the presence of lobsters aamd represents a defence rnecha- nism against predation. This mechanism explains how srnall clearings begin appearing in otherwise healthy-looking Lami- nariec beds. Depending on the relative densities of urchins and lobsters, these clearings would then either disappear and reap- pear in a shifting mosaic or persist and enlarge as more and more urchins aggregated. This latter scenario fits the observed progression of kelpbed destruction in St. Margaret's Bay, Nova Scotia. In that instance, ciearings associated with urchin grazing persisted and enlarged until most of the bay had been denuded sf kelp (Breen and Mann 1976; K. H. Mann, personal observation). In addition, the fact that urchin clunaps were larger in the winter corresponds with observations that destructive feeding aggregations most often form in late fall and winter, probably kcause large predatory fish arc absent during those seasons (Bernstein et al. 198 1).

A key feature of destructive feeding aggregations is that they represent a behavior that permits urchins to forage openly. even in the presence of predators (lobsters). Our data show that, in fact, urchins in open subhabitats clump much more in response to lobsters than do those in cryptic subhabitats. For the percentage clumped variable, the habitat x density x predators interaction was statistically significant for urchins in the open, but not for those in hiding (Table 3). For the mean clump size variable, the treatment means (Table 6) indicate that, at high urchin density in the kelp, with lobsters. mean clump size was 2.4 for urchins in the open and only 1.8 for urchins in hiding. Similarly, the percentage clumped was 61% for urchins in the open and only 43% for urchins in hiding.

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1982 CAN. J . FISH. AQUAT. X I . , VOL. 40, 1983

r BARRENS 2 ea- 8 Q 0

g 4 a -

c; u ; 20- 2 bb) dl

a W L O

HLGH DENSITY L W DENSITY

CRABS NONE

LOBSTER I

FRBM KELPBED, SUMMER

HIGH DENSITY LQW DENSITY

HIGH DENSITY

FROM EELPBED, WINTER

L O BARRENS KELPBER

HABITAT HABITAT

lz lL

I 2. Interaction plots of the habitat X density X predators interaction for the variables (A) mean clump size for a11 urchins in the FROM FROM

BARRENS KELPBED cage, (B) percent clumped for all urchins in the cage, and ( C ) percent clumped for urchins in the open. This interaction was stat<stical8y significant for all three variables (Table 3). Ciumping is always greater at high urchin density, and this effect is enhanced in the presence of lobsters in the kelpbed. In contrast, clumping in the barrens at high urchin density is always greatest in the presence of crabs. The degree of clumping thus depends on t h particular combination of the three factors. See Tables 5 and 6 for further analysis of the treaement means.

We had earlier proposed (Bernstein et al. 1981) that crabs were responsible for indusing urchin clump formation in kelpbeds. We based this suggestion on our observation that crabs induced clumping in the laboratory as a defence mechanism. The present series of experiments demonstrates that urchins will not clump in response to crabs in the kelp, but only in the bmens. Because there was no kelp in the laboratory experiments, these mare closely resembled the bmen habitat.

Three other significant interactions described additional effects sf the factors season, source, habitat, and density on clumping behavior (Table 3). These are season X habitat x density, source X habitat X density, and season X source X

habitat X density (Fig. 3A). Since the factors involved in the first two are included in the third, we discuss only this last interaction. It shows (Fig. 3A) that urchins from the barrens clump more in the kelp at low density during the summer than

FRBM BARRENS SUMMER

FROM BARRENS, WINTER

DENSITY

BARRENS HUBITAT

I KELPeER HABITAT

FIG. 3. (A) Interaction plot of the season X source X habitat X

density interaction for percent clumped for all urchins in the cage. The pattern of clumping is similar across all conditions, except for the anomalously high clumping of urchins from the bmens at low density in the kelpbed during the summer. (B) Interaction plot of the source X predators interaction for the percent of urchins in hiding. Urchins from the kelpbed hide more in the presence of crabs than do urchins from the barrens. The source of urchins has no effect on clumping in the iobster and control treatments.

in any other treatment. This is the only instance when the percentage slumped at atow urchin density exceeded the percentage claam@ at high urchin density. This was not a response to predators, since the urchins were clumped on a Laminaria blade. It could have resulted from the increased f w d supply represented by the Laminaria plants In the cages. We have observed that urchins in the barrens will quickly aggregate and feed on drift hmbnariacb. G m i c k (1978) and K. W. Mann and B . E. Welsford (Bedford Institute of Ocean- ography, P . 8 . Box 1006, Dartmouth. N.S. , unpublished data) have demonstrated that urchins will heme on the scent released by mother urchin feeding on Laminaria. If one of the four urchins in the low-density treatment began feeding first, it is likely the others would have aggregated on it, resulting in a high figure for percentage clumped. At high density, there

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BERNSTEIN ET AL.: SEA URCHIN AGGREGATING BEHAVIOR

IN KELPBED, SUMMER IN BARRENS, SUMMEW because they were well fed. BSTER

HIDING

Hiding is an alternative antipredator defence and is com- plementary to the aggregating behavior described. We found that urchins were more likely to hide in the summer than in the winter (Tables 3 and 41, most probably because large predatory fish are common in the summer but not in the winter, and only very large aggregations are an effective defence against these fish (Bernstein et a!. 198 1). Season was also involved in a higher level interaction (season x source x density) (Table 3). While significant, the effect was small relative to other interactions, and we therefore do not treat it further.

w

8 IN KELPBED, WINTER Urchins frorn the kelp and bmens also exhibited different

9 80 I N BARRENS'W'NTER hiding behavior. Urchins from the kelp hide more in the

0 LOBSTER Z

presence of crabs than do urchins from the barrens (source x

S predators) (Table 3; Fig. 3B). This is understandable in view

g 60 of the fact that urchins in the barrens ciaamp as a defence

CRABS - - - ~ ~ ~ ~ s against crabs, while urchins in the kelp do not. Some aspects z of urchins9 response to crabs may thus be entrained by the 8 tx habitat urchins live in and persist even when they are moved W 4 0 61 to another habitat. There was no analogous hiding response to

\ \

lobsters. \ \

20 \ ' NONE ~/LOVEMENT

0 H6H DENSITY LOW DEHSlTY HIGH DENSITY LOW DENSITY

FIG. 4. Interaction plot for the season X habitat X density X predators interaction for the percent along the wall for all urchins in the cage. Except for the summer in the kelpbed, percent along the wall is higher at low than at high urchin density, when predators are present.

would be several urchins feeding on &urninaria sirnulta- neously , with several sources of scent. Urchins would thus be dispersed around the cage. Urchins frorn the kelp did not exhibit this low density aggregation response, presumably

Movement, or fleeing, is a third potential antipredator strat- egy. Like clumping, it can result from bath foraging and antipredator behaviors. Mattison et al. ( %977), working with Strongybscentrstus franciscanus, showed that urchins in a b m e n area moved farther than those inside a kelpbed. They interpreted this as foraging behavior in an area with a Bow concentration of food. The percent of urchins in a cage along the wall reflects the degree of movement in the cage. Urchins fleeing from crabs or lobsters in the cage are more likely to be along the wall. Similarly, urchins attempting to forage along the boundaries of the cage will concentrate along the wall. Figure 4 shows that the percentage along the wall in the crab

TABLE 5 . Means and ranges (in parentheses) of the largest urchin clump in each replicate of the treatments in the significant habitat X density X predators interaction. Owiy at high urchin density in the kelp with lobsters and in the barrens with crabs do clumps larger than 10 occur.

Habitat Density Predators n Total o ~ n Cryptic

Kelpbed High Grabs Lobsters None


B m n s High Crabs Lobsters None

b w Crabs Lobsters None

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CAN. J . FISH. AQUAT. SCI., VOL. 40, 1983

TABLE 6. Treatment means averaged across source and season for the habitat x density X predators interaction (Fig. 2). Largest clumps occur in the kelpbed, at kigh urchin density, in the presence of lobsters, in the open.

Mean clamnap size Habitat of Density experiment of urchins Predators PI Total Open Cryptic

Kelpbed High Crabs Lobsters None


Barrens High Crabs Lobsters None


and lobster treatments is generally higher at Bow than at kigh urchin densities. Urchins at low density are more likely to attempt to flee, since the clumping defence is not available to them. This, in fact, reflects what happens when urchins are placed into a healthy kelpbed with very low natural urchin densities: they rapidly disperse (Breen and Mann 1976; B. B. Bemstein, personal observation). Table 3 shows that predators do not affect the percentage along the cage wall of urchins in hiding, but only of those in the open. Urchins in hiding are presumably relatively safe from predation m d respond only to habitat (Table 3). More s f them, however, are found along the wall in the barrens than in the kelp (Table 4). Since this is not a response to predation, it implies that urchins in the barrens forage more widely than do those in the kelp, even when they are in hiding. They we able to remain in hiding because many of the spaces between the bo~lders are interconnected and act as traps for drift algae.

The interpretation of our results is contingent on an identi- fication and understanding of any potential biases resulting from the cage treatments. There rare three issues to consider: (1) do the cages affect the physical-chemical environment and thus urchin behavior, (2) do the cages affect the physical-chemical environment in the control and predator treatments differently, and (3) is there an interaction between cage effects and urchin behavior in the different treatments that would arkificially create or mask the effects we are studying'?

Cage effects on the physical-chemical environment and thus on urchin behavior could have resulted from interference with water movement, the provision of added environmental heterogeneity and structure, and restriction s f the animals' normal movement patterns. We utilized monofilament mesh for the cage walls because it interfered minimally with water movement. Its flexibility also prevented urchins from

climbing up the walls, which they did with stiffer materials. We also minimized the cage structure as much as possible to avoid interfering with the natural habitat. Urchins came into contact only with the monofilament mesh wall. They behaved towad the wall as they did toward other habitat structure, i.e. they occasionally sheltered under it. Effects from the cage stmcture were minimal; we observed no abnomal behavior in the cages by either urchins or predators. Since all cages were identical, and replicates of treatment were performed in different cages, there is no reason to assume any consistent difference between controls and predator treatments.

The key issue is the third one mentioned above, 1.e. whether there are interactions between cage effects and urchin behavior in the different treatments that would create or mask the aggregating behavior we were studying. Qne such poten- t id interaction did concern us. The cages did restrict urchin movement, especially in the high-density treatments in the kelpbed. Without the cages, the urchins would have dispersed. We considered the possibility that urchins clumped in the presence of lobsters only because they had attempted to flee and could not. In a natural situation with widespread high urchin density, however, urchins from a small area would not be able to disperse. As they began to do so, densities would become locally enhanced, and clumping would be speeded because of the density effect. We found, however, that tbe percent of urchins dong the cage wall is completely uncoare%ated with mean clump sizes. This indicates h a t the clumping response, the main focus of interest, acts indepen- dently of any dispersal, or wall, effect.

In addition, the results we obtained at Green Island ape almost identical to those we obtained in a pilot experiment near Halifax (Tables 7 and 8) where the presence of crabs was associated with significantly larger clumps. Clump sizes were larger in this pilot experiment most probably because there were four large crabs per cage, rather than two. Finally, the clump sizes, and the rapidity of the aggregation response, agree with our laboratory results reported in an earlier study (Bernstein et al. 1981). We are therefore confident that there is no serious bias in o w experimental results.

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BERNSTEIN ET AL.: SEA URCHIN AGGREGA~NG BEHAVIOR 1985

TABLE 7. Treatment means of pilot experiment in the barrens to test for the presence of clumping in the field. Cages were about B m'. a , mean clump size; &, % clumped.

Substrate

Sand Wwk

Crabs Density a b n b

Without 5 2.4 46.7 1.3 40.0 Without I0 2.2 74.0 2.0 65.7 Without 10 1.8 63.3 2.5 76.3 Without 15 1.3 42.0 With 15 2.7 86.8 3.5 90.7

We found that urchin aggregating behavior is extremely flexible and is responsive to changes in several important environmental parameters. These responses are probably mediated by urchins' sensitivity to biochemical cues. Garnick (1978) has shown that S. droebachiensis in the laboratory can consistently discriminate among combinations of cues from other urchins, Lumincaaia, and urchins feeding on Earninaria. Urchins respond to these cues by moving toward them. and respond m s t strongly to other urchins eating Laminaria. K. H. Mann and B. E. Welsford (unpublished data) have demonstrated that urchins9 behavioral response to Laminaria depends on their sensitivity to small, volatile meslecules (1800- 10 000 MW) released by Lamistaria. They have also established that S . droebachiensis flees from lobster and crab scent in laboratory Y-tube experiments.

This sensitivity allows urchins to respond to changes in their environment that have clear adaptive significance, i.e. the opportunity for increased food, or the risk of increased predation. What the present experiments, as well as our previous work (Bernstein et al. 198 11, demonstrate is that the intensity and type of urchin defensive responses to predators are adjusted to the intensity and type of predation. For example, urchins hide when large predatory fish are present, and only form exposed feeding aggregations in the presence of these predators at extremely high densities (80 a m--2). Urchins zlso hide in the presence of lobsters, but will begin forming exposed defensive aggregations when their density surpasses 20.11-'. Ian each instance where aggregations form, their effect is to allow urchins to forage openly while minimizing the risk of predation. We have shown previously (Bernstein et al. 1981) in laboratory experiments that large crabs are much less successful attacking urchin aggregations than they are attacking individual urchins, even when these individuals are well sheltered in rocks. Crabs find it impossible to encircle an aggregation with their claws; in effect, it is one huge urchin. While we have no analogous documentary evidence for lobstern, we hypothesize that aggregations provide urchins with similar protection from lobsters. Aggregation is thus a more effective defence than hiding. because both crabs and lobsters can readily enter the spaces between the boulders.

The formation of these aggregations depends not only on urchin density and predators, but also on habitat type. Urchins aggregate in response to lobsters in the kelpbed, but to crabs in the bamens. This implies that there is some qualitative

TABLE 8. Effect of crabs, urchin density, and habitat on mean urchin clump size and % cclumpd, tested by ANOVA. Clump sizes transformed to log,o (x + 1) sf clump size, and O/n clumped transformed with arc sine square root. *P < 0.05.

Sums of Mean Variable Source df squa~es square F

Clump size Crabs Density Substrate Residual

% clumped Crabs Density Substrate Residual

difference between lobster and crab predation, that perhaps lobsters forage more effectively in kelpbeds, while crabs forage more effectively in the barrens. There is, unfortunately, no detailed information on the relative abundance, rnicro- habitat utilization, or foraging tactics of these two predators in barrens and kelpbed habitats.

The kelpbed-barrens ecosystem exhibits a radical shift between two clear-cut states. The kelpbed state is chxacter- ized by persistent and dense cover of the large kelps, Lami- naris sp., with an understory of Ckondru~s' and other f o m s , and the presence of few sea urchins ( S . droebachr'erasis) (<5. m-') (Mann 1972; Bemstein et al. 198 1; Wharton and Mann 1481). The b m e n state is characterized by an almost complete absence of macroalgae and abundant encrusting cop- alline algae. Sea urchin densities are much higher than in the kelp (20-30*m-2), and the urchins act to maintain the barrens by grazing any Earninaria that resettle (Chapman 198 1 ; Bemstein et al. 1981; Whaton and Mann 1981). There is abundant evidence that dense aggregations of urchins at extremely high densities (80- 108.m-2) are the mechanism that transforms the kelpbed into barrens by destructively over- grazing the kelp (Breen and Mann 197'86; Mann 1977).

We believe that the experiments described above demonstrate the operation of a behavioral mechanism that is the trigger point for this large-scale change in community structure. Urchins at Isw density in a healthy Laminaria bed remain in hiding. When urchin density passes a critical threshold at about 20- rn-2, they begin forming small clumps in the open. As lobsters begin feeding on these clumps, urchins' defensive aggregating response precipitates the sudden formation of even larger clumps, destructive grazing of the kelpbed begins, and bamens ultimately form.

Predation has complex effects .in this system. Fish, crabs, and lobsters affect the intensity of urchin grazing differently Most importantly, the same predators (lobsters) have completely opposite effects on the intensity of urchin grazing, depending on urchin density. Lobsters have no effect at Iow urchin density, but catalyze a dramatic aggregation response in the urchins above a threshold density. This defensive clumping is analogous to the fornation of flocks or schools in other species (e.g. fish). Defensive aggregating behavior in urchins shifts the relative intensity of the mortality urchins are

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1984 CAN. J . FISH. AQUAT. SCI., VOL. 40, 1983

exposed to by lowering the intensity of predation. Urchins appear to shift among the several behaviors available to them, based o n a combination sf conditioning and a rapid response to biochemical cues, including those from algae, predators, and other urchins. This entire process, including its large- scale end result, is therefore understandable in terms of the behavioral responses o f individual organisms to immediate selective pressures.

Acknowledgments

We thank Randall Angus, John Stairs, and Solange Brault who carried out the field operations, often under difficult conditions, and Don Peer and Ken Freeman who monitored pmgress on behalf of the Bepartnaent of Fisheries and Oceans. We also thank P. K. Dayton and W. T. Paine for helpful comments on the manuscript.

BERNSZIN, B. B., B. E. WILLIAMS, AND K . H. MANN. 1981. The role of behavioral respmses to predators in mdifying urchins' (Strong~iocenrrobus droebcachiensis) destructive grazing and seasonal foraging patterns. Mar. Biol. 63: 39-49.

BWEEN, P. A., AND K. H. MANN. 1976. Destructive grazing of kelp by sea urchins in eastern Canda. J. Fish. Res. Board Can. 33: 1278- 8283.

CHAPMAN, A. R. 0. 1981. Stability of sea urchin dominated barren grounds foilowing destructive grazing of kelp in St. Margaret's Bay, eastern Canada. Mar. Biiol. 62: 387-312.

GARNICK, E. 1978. Behavioral ecology of Strongy%ocentrotus droe-

kchiensis (Muller) (Echindermata: Echinoidia). Oecologia ( B e r m 37.- 77-84.

GREEN, R. %I. 1979. Sampling design and statistical methods fur environmental biologists. John Whley & Som, New York, NY. 257 p.

HARRIS, R. J. 1975. A primer of multivariate statistics. Academic Press, New Ysrk, NY.

MANPI, K. H. 1972. Ecological energetics of the seaweed zone in a marine bay on the Atlantic Coast of Canada. I. Zonation and biomass of seaweeds. Mar. Biol. 12: 1 - 10.

1977. Destmction of kelp-beds by sea urchins: a cycli- cat phenomenon or irreversible degradation? Helgol. Wiss. Meeresunters. 30: 455 -467.

MAITISON, 1. E. , J. C $ . TRENT, a. L. SHANKS, T. B. AKIN, AND J. S. PEARSE. 1977. Movement and feeding activity of red sea urchins (Strcpn,qylocenrrotus frcanci.~ccan~ds) adjacent to a kelp forest. Mar. BioH. 39: 25-30.

SNEDEGOW, G . W., AND W. G~ CWHRAN. 1967. Statistical methods. Iowa State University Press, Ames, IA. 593 p.

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UNDERWOOD, A. %. 1981. Techniques of analysis of variance in experimental marine biology and ecology. Oceaaagr. Mar. Biol. Annu. Rev. 19: 513-605.

MIMARTON. W. G., AND K. H. MANN. 1981. Relationship between destructive grazing by the sea urchin, Srro.canggbocenrroruss droehckiensis, and abundance of American lobster, Hornerrus ameriwnus, on the Atlantic coast of Nova Scotia. Can. %. Fish. Aquat. Sci. 38: 1339-1349.

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sea urchin (strongylocentrotus droebachiensis) aggregating behavior investigated by … ·...

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