Seasonal changes in calorific value of three pacific coast seaweeds, and their significance to some marine invertebrate herbivores

J. e.vp. ~r~nr.Biol. Ecol.,

SEASONAL PACIFIC

1975, Vol. 18, pp. 139-151; >Q North-Holland

CHANGES

COAST

IN CALORIFIC

SEAWEEDS,

VALUE

Publishing Company

OF THREE

AND THEIR SIGNIFICANCE

TO SOME MARINE INVERTEBRATE

HERBlVORES

JOHN H. HIMMELMAN and THOMAS H. CAREF~~T Deportr?rent of Zoology, Unicersity of‘ British Colambiu, Vnncoucer, Canada Abstract: Samples of three intertidal seaweeds, Iridaea corduta (Turner) Bory, Hedophyllum sessik (C. Agardh) Setchell, and Lessoniopsis littoralis (Farlow and Setchell) Reinke, collected at nine intervals over the period May 1971-May 1972, showed statistjcaiiy significant seasonal fluctuations in percentage dry weight, percentage ash content, and calorific value. Percentage dry matter was generally highest in late summer through winter, whereas ash content was low. Ali three species showed a distinct annual cycle in calorific value of live (damp-dried) material, being highest during August-February for Hedophyllum and Iridaea, and during August-December for Lessoniopsis. Calorific values of dry material similarly varied seasonally for all species, but the differences were not significant for Iridaea. On an ash-free basis, the calorific values of ~edo~hyilum and Iridaeu were variable during the year, and only Lesso~io~sis showed significantly higher values in late summer and autumn. The seasonal variability in calorific value of seaweeds has important implications in the feeding ecology of certain invertebrate herbivores. For example, while the chiton, Katherina tunicata Wood, consumed less Hedophyllum in the autumn than during the spring and summer, caloric intake did not decrease proportionately due to an inverse cycle in calorific value of tIedoph_vllum. In addition, we discuss for a number of invertebrate herbivores their feeding preferences, and the importance of calorifrc value of seaweeds and other factors which may have been involved in the evolution of these preferences.

INTRODUCTION

In the temperate latitudes, marine algae undergo distinct seasonal cycles in growth and reproduction which involve numerous biochemical and other changes. A number of studies have shown seasonal variations in dry weight, ash weight, and in the composition of various constituents in marine algae (Butler, 1936; Black, 1950; MacPherson & Young, 1952; Wort, 1955; Baardseth, 1970). Few studies have, however, provided data on seasonal cycles in calorific value of seaweeds. Paine & Vadas (1969) could find no evidence of seasonality in their data on calorific values in a number of Pacific Coast seaweeds. Mann (1972) also found no seasonal variation in calorific value of dry material in his study of the seaweeds of St Margaret’s Bay, Nova Scotia, but did predict seasonal changes in calorific value on a live-weight basis. The present paper deals with seasonal variations in the content of ash, dry weight, and calorific value of three North American Pacific Coast seaweed species: the red alga, Iridaea cordata (Turner) Bory, and the brown algae, Hedophyllum sessile (C. Agardh) Setchell and Lessoniopsis liftoralis (Farlow and Setchell) Reinke. 139

140

JOHN H. HIMMELMAN

In addition, black

seasonal

leather

chiton,

variations

AND

THOMAS

H. CAREFOOT

in food consumption

Kutherina tunicata Wood

and caloric

are discussed,

intake

in the

and consideration

is

given to other benthic invertebrate herbivores from data in the literature. In particular, we are interested in the relationship between attractiveness of a food material to a herbivore edibility,

and its nutritional

and its use for growth

quality

measured

by e.g., its calorific

value,

its

and reproduction.

MATERIALS AND METHODS

COLLECTIONS Nine collections of algae were made at monthly or bimonthly intervals between May 1971 and May 1972 at Botanical Beach, Vancouver Island, British Columbia. This area is at the entrance to the Strait of Juan de Fuca and faces the open Pacific Ocean in a westerly direction. The algae were collected from a ledge which sloped gently into the sea. Hedophyllum sessile and Zridaea cordata were collected 0.5-1.5 m above E.L.W.S. tidal level where they were the predominant littoralis was collected from just below this level.

plant forms; Lessoniopsis

Portions of the blade weighing 5-10 g were taken from each of five different plants of each species for each collection. These samples were damp-dried, weighed, and initially dried in a propane oven at 80-90 “C in the field. They were then kept in a sealed jar with desiccant for a day or two until they were further dried in an electric oven at 90 “C for 48 h. The dried material was stored with desiccant at - 15 C. CALORIMETRYAND ASHING The calorific value of each sample was determined by combustion in a Phillipson microbomb calorimeter. Pellets of 8-20 mg were formed from portions of each homogenized sample. The calorimeter was calibrated with benzoic acid. Each unknown was replicated. Percentage

ash was determined

by heating samples

of each seaweed

at 450 “C for

12 h. These ash data allowed comparisons to be made on the basis of calorific value of the combustible component of the sample alone. FEEDING EXPERIMENTS Kutherina tunicata usually attaches firmly to rock surfaces. It may lifl its anterior end, as when it feeds, but it very seldom if ever is without at least its posterior foot portion fastened firmly. Because of this behaviour it was possible to keep animals enclosed in small areas (about 900 cm2) surrounded by a plastic mesh fence 8 cm in height. Ten experimenlal enclosures were erected on a relatively flat area in the Hedophyllum sessile zone at about 0.8 m above E.L.W.S. tidal level (Fig. 1). Within each enclosure all algal growth was removed and a central bolt was cemented to the rock, screw end up. Pieces of H. sessile or Zridaea cordata, of uniform thickness and cut into square or rectangular shapes, were placed over the bolts, one per enclosure,

SEASONAL

Fig. I. A feeding effects of feeding

CHANGES

IN

CALORIFIC

VALUE

enclosure at Botanical Beach, Vancouver Island, by the chiton, Katherina tunicuta, on the brown a 24-h period (July, 1972).

OF

SEAWEEDS

British Columbia, showing the alga, Hedaph.sNum scssile, over

through a hole punched in the center of each piece. Plastic washers and wing nuts held the algal pieces close to the rock surface. Katherina were kept in such enclosures for up to six months. In many instances within a short time they adopted homing areas in depressions of 1he rock surface, in corners or under the attached algae. Adult Katherina, of a live weight range of 30-50 g were used in separate experiments to determine seasonal variations in feeding rate on ~ed~~h~li~~~ sessile. Each individual animal was maintained in an enclosure with ample food for at least a week prior to measuring the feeding rates. During a feeding experiment, lasting for 2-10 days, the pieces of algae were changed daily. Whenever a portion of blade had been eaten an equivalent portion of remaining blade was weighed to measure how much was eaten. Loss of food material resulting from the rasping method of eating was not measured, but we do not believe that it was significant, or that it was other than in direct proportion to the amount consumed, and so not affecting our seasonal comparisons. The feeding behaviour of Kctherina was highly variable and an animal might feed in extended sessions once or twice a day, or not at all for a few days. When nothing was eaten the zero values were included when calculating feeding rates if they occurred between days when the animal was feeding and if there were no reason to suspect the animal was not healthy.

JOHN H. HIMMELMAN AND

142

THOMAS

H. CAREFOOT

STATISTICAL ANALYSES The data on dry weight, ash content, and calorific value were plotted for each alga seasonally. In many instances the variances were heterogeneous, being greater in some seasons (frequently autumn and winter) than in others. The Kruskai-Wallis one-way analysis of variance by ranks was used to test !he null hypothesis that there was no difference in the average values of samples collected at different times in the year.

RESULTS DRY

WEIGHT

The null hypothesis that there was no difference among the samples collected in different months was rejected (P < 0.01) for each seaweed, and from Fig. 2 it is clear that the variation occurred in a distinct seasonal pattern throughout the year. Each species showed a maximum in dry weight from August through early to late

.

0

I

MAY

I1

JUL

I

I

SEPT

1971

I

I

NOV

I

I

JAN I

I

I

MAR

1

I,

MAY

1972

Fig. 2. Percentage dry weight of Iridaea cordata, ~edop~~yl~~~lsessife, and Lessu~jopsjs littoralis as a function of time: in this and Figs 3-6 each point represents the mean of five different samples and the vertical bars 95 ‘A confidence limits.

winter. For Iridaea Ihe maximum was 28 x, dry weight in August-March pared with 22 % for the other months; for Les~on~opsis, the maximum for August-December as compared with about 18 “/, for the other months, the January value because of its intermediate position; for Hedophyllum, mum was 18 % for August-February as compared with about 12 y0 for months.

as comwas 25 y/i excluding the maxithe other

ASH WEIGHT

The seasonal changes in percentage

ash weight are shown for each species in

SEASONAL

CHANGES

IN CALORIFIC

Fig. 3. The three species showed significant through

October-December;

maxima

VALUE

OF

(P < 0.01) seasonal

occurred

during

143

SEAWEEDS

minima

the period

from August

January-March

to July. All the Iridaea collected in October were < 25 ‘4 ash weight, while those collected from February through July were all > 25 “/,I ash weight. Lessoniopsis

10-p MAY

JUL

SEPT

1971

Fig. 3. Percentage

ash weight

of Iridaea

NOV

JAN I

MAR

MAY

1972

cordata, Hedophyllum a function of time.

sessile,

and Lessoniopsis

littoralis

as

collected in August and October ranged from 16-22 % ash weight, compared with 24-29 % for material collected in the other months (excluding December which was intermediate). Hedophyllum values were all > 32 % ash weight during the period March to May, whereas 9 of the 10 plants collected in the months of October and December were < 28 % ash weight. Of the three species, H. sessile showed the most distinct annual cycle. CALORIFIC

VALUE

The calorific values of the three seaweeds are shown as kcal/g live material in Fig. 4, as kcal/g dry matetial in Fig. 5, and as kcal/g ash-free material in Fig. 6. The most consistent and distinct annual cycle is shown when the calorific value is expressed

on the basis

of live weight

(Fig. 4), with highest

values

in the summer,

autumn, and in two of the species, in the early winter months (all significant at P < 0.01). Values for Iridaea were 0.70-0.98 kcal/live g in August-February and 0.56-0.70 kcal/live g in May and June. For Lessoniopsis the values ranged from 0.67-I .23 kcal/live g in August-December, compared with 0.44-0.63 kcal/live g during the other months. All the Hedophyllum collected during the period MarchJune had < 0.43 kcal/live g of tissue whereas 18 out of 20 plants in August-February had > 0.43 kcal/live g of tissue. When the calorific value is expressed on the basis of dry weight the distinctive seasonal differences shown in Fig. 4 are less apparent (Fig. 5), since percentage dry

144

JOHN

H. HIMMELMAN

MAY

JUL

AND

SEPT

THOMAS

NOV

values/g

MAR

JAN

MAY

1972

1971

Fig. 4. Calorific

H. CAREFOOT

live weight of Iridaea cordara, Hedophyllurn littoralis as a function of time.

sessile,

and

Lessoniopsis

weight is positively correlated with calorific value of live material. For Zriduea the monthly samples did not differ significantly (P > 0.05) although the cyclical pattern of the data (Fig. 5) suggests that seasonal differences would be present with larger sample sizes. Both Lesxkopsis and Hedophyllum, while still showing statistically significant late-summer and autumn maxima (P < O.Ol), nonetheless have less distinctive annual cycles following the conversions from kcaljlive g to kcaljdry g (Lessoniopsis: 3.5 kcal/dry g during August-December, as compared with 2.8 kcal/ dry gin the remaining months; Hedophyllum: 3.2 kcal/dry g during August-February. as compared with 2.6 kcal/dry g in April and May).

2’MAY’

’

JUL

’

’

1971

Fig. 5. Calorific

values/g

dry

’

SEPT

’

NOV

’

’

JAN

I

’

’

MAR

’

’

MAY

’

1972

weight of Iridaea cordara, Hedophyllum littoralis as a function of time.

sessile,

and

Lessoniopsis

SEASONAL

CHANGES

IN CALORIFIC

VALUE

OF SEAWEEDS

145

Calorific value of ash-free dry matter showed less seasonal variation (Fig. 6) than did calorific value of dry matter due to the inverse correiation of high ash content with low calorific value of dry material. The difference between the monthly samples was not significant for either Zridaea or Hedophyllum (P > 0.05). For Lessoniqsis, however, the monthly samples did differ significantly (P < 0.01) and

MAY

JUL 1971

SEPT

NOV

JAN i

MAR

MAY

1972

Fig. 6. Calorific values/g ash-free dry weight of Iridaea cordata, Hedophyllum sessile, and Lessoniopsis liftoralis as a function of time.

a distinct seasonal cycle was still evident. Nine out of the 10 plants collected in August and October had greater than 4.2 kcal/g ash-free matter, compared with values less than 4.0 kcal/g ash-free matter for all samples collected in February and March. FEEDING

EXPERIMENTS

The seasonal feeding rate of Katherina tunicata on Hedoph_vll~m sessile is given in Fig. 7. There are significant seasonal differences (P < 0.01) in the rate of food, intake in spite of the markedly irregular feeding habits of this animal. For example, the mean rates recorded in October and December, 1971 (0.3 and 0.6 liveganimal-’ day-‘, respectively), were one half to one third the rates recorded during the period May-July, 1972 ( I. 1-I .4 live g animal- 1 day-‘). The rate decreased rapidiy in September of 1971 and again in August of 1972. A comparison of the feeding rate of Katherina on Zridaea during July 1972 showed that 0.39*0.11 (95 % confidence limits) g live weight of Iridaea was eaten per animal per day. Note that this rate was only one-third that on HedophyiIum in July. During July-September 1972 the preference of K~theri~a for Hedop~yi~um and Zridaea was investigated. Pieces of Hedophyllum and Zridaea were attached to separate bolts within the same enclosure so that both algal species were accessible to the

146

JOHN H. HTMMELMAN

AND THOMAS H. CAREFOOT

1 0

AUG

“““‘1”1’1

DEC

OCT

1971

FEE

JUN

APR

AUG

1972

I

Fig. 7. Feeding rate of the black leather chiton, Kutherina tunicata on Hedophyllunt sessile at different times of the year: means based on 840 observations: 95 % confidence limits are shown.

chiton. In a total of 13 1 daily trials Hedophyllum alone was eaten 86 times, Iriduea alone 28 times, and pieces of both algae were eaten 17 times, suggesting a strong preference for Hedophyllum. In addition, in 10 trials when the positions of the attached Hedophyllum and Iridaea were switched in enclosures where the chitons had been eating Hedophyllum, the animals continued to eat Hedophyllum five times in spite of its new location. In three instances both were eaten, and in two instances feeding stopped for l-2 days.

DISCUSSION SEASONAL

CHANGES

IN SEA’WEEDS

It was not unexpected tissues of these temperate reproduction

to find seasonal variations in the calorific value of the seaweeds. The distinct seasonal periods of growth and

and the related

biochemical

changes

would

support

such an a priori

assumption. While there is ample evidence of seasonal cycles in chemical composition of seaweeds (Butler, 1936; Black, 1950; MacPherson & Young, 1952; Wort, 1955) no one to our knowledge has yet found seasonal cycles in calorific value of seaweeds. Paine & Vadas (1969), for example, were unable to find seasonal variations in calorific value of ash-free material in a number of Pacific Coast seaweeds, including Hedophyllum senile and an unidentified species of Iridaea. While fully supporting their results (assuming that the various Iriduea species are similar in their calorific value), we did find a definite seasonal cycle in calorific value of live material for Hedophyllum senile and Iridaea cordata, and have shown that there is also a seasonal cycle for the former species on a dry-weight basis. Mann (1972) found little and inconsistent seasonal variations in the calorific value of dry matter of Laminaria

SEASONAL

CHANGESIN

CALORIFIC

VALUE

147

OF SEAWEEDS

longicruris, L. digitata, and Agarum cribrosum from St Margaret’s

Bay, Nova Scotia,

but concluded

and calorific value

on the basis of distinct

differences

in water content

of dry material that there must be a marked seasonal change in calorific value of the fresh plant material. Our data on calorific value of live material show clear and consistent material,

seasonal

trends

for each species.

while the same seasonal

trends

On the basis of calorific

are evident

value

of dry

for the two phaeophytes,

the

Zridaea cycle becomes masked. Finally, on the basis of calorific value of ash-free material, only Lessoniopsis littoralis retains its original seasonal cycle. It is probable that the seasonal cycles of dry weight, ash content, and calorific value are related to chemical and morphological changes associated with the various phases of reproduction and growth. Spores are presumably rich in ‘energy’ and one might expect higher calorific values in spore-bearing tissues. Lessoniopsis and Hedophyllum were sporulating in late autumn and winter and fertile fronds of Zridaea predominated from late summer through winter; the calorific values were highest during these reproductive periods. The seasonal calorific cycle was least distinct for Iridaea, but the presence of isomorphic sporophytic and gametophytic stages, at the same time, in various states of fertility, probably increased the variability of our data. One Zridaea plant collected in August and another in October were not fertile and had lower calorific values and higher ash values than did the other fertile plants collected at the same time. Also, in December one female plant with carpogonia had a higher calorific value (per dry g) and lower ash conient than did the four other plants with tetrasporangia. This supports the suggestion that reproductive tissues, especially female reproductive tissues, may have higher calorific value than non-fertile tissues. In all three species, maximal growth was from March to August when the photoperiod was longest. Perhaps the seasonal changes in calorific value of dry material could be related to variations in the content of lipid or other high-energy material in the tissues during the different growth stages. In this regard, Wort (1955) reported highest

concentrations

of ether-soluble

material

in the brown

Zuetkeana, to be present in March, and lowest during difference to low levels of “fat” (ether-soluble material) active

growth,

with later accumulation

in mature

alga,

Nereocystis

June-July. He related this during the period of most

plants.

Unfortunately,

we have

no data on tissue lipid content to substantiate this idea. In summary, low dry weight, low calorific value, and high ash content in the spring and early summer were coincidental with maximal growth. Reproductive products were being produced in the late summer, autumn and early winter coincidental with high dry weight, high calorific value, and low ash content. At present we can offer no sure biochemical basis on which to relate these phenomena. SEASONAL ASPECTS OF FEEDING BY Katherina tunicata AND

OTHER

BENTHIC INVER-

TEBRATE HERBIVORES

Katherina consumed

nearly

three times more

live weight of Hedophyllum in the

JOHN H. HIMMELMAN

148

spring

than

in the autumn:

however,

much less since the calorific

AND

THOMAS

the seasonal

H. CAREFOOT

variation

in caloric

intake

value of Hedophyllum was low when feeding

high, and high when feeding rate was low. As a result, an animal of Hedophyllum in the autumn

would

have a daily caloric

eating 0.5 live g/day

intake

(Fig. 7). In comparison, in the spring, the daily consumption provide about 0.4 kcal. In some invertebrates, as for example

was

rate was

of about

0.3 kcal

of 1.2 live g would sea urchins, less food

is consumed as the spawning period draws near. Katherina, however, was feeding at its highest rates in May and June just at the time of spawning. Seasonal cycles in feeding activity are characteristic of most benthic marine invertebrates in temperate climates. Perhaps more information is available for sea urchins than for any other benthic invertebrate herbivore. In Japan, Fuji (1967) found that adult Strongylocentrotus intermedius (55 mm dia.) consumed about 3 live g Laminaria aponicalday from December-June, and only z 1 live g/day from July through October. Although the high consumption rates corresponded to some extent with low temperatures they were correlated more closely with the reproductive cycle of the sea urchin. Least was eaten in the autumn period when the urchins were ready to spawn; after spawning feeding rates increased markedly. If the calorific value of Laminaria ,japonica follows a similar seasonal pattern to what we found for the seaweeds in our study - namely, low values in spring and early summer, and high values during late summer and autumn - this would to some extent offset the lower caloric intake in the autumn due to the lower feeding rate. In Newfoundland, Strongylocentrotus droebachiensis similarly showed a marked seasonal variation in the rate of food consumption (Himmelman, 1969); e.g., adult animals (50 mm dia.) ate 1.0 live g Laminaria (mostly L. longicruris but may have included some L. saccharina)/day in February, and 2.2 live g/day in May. During this period the temperature increased only slightly. Since the sea urchins spawned in April it is possible that the consumption cycle was related to the reproductive cycle. Mann (1972) found that the dry weight of blades of L. Zongicruris from shallow water varied up to 80 % seasonally, with maximal values in the late spring and summer. whereas calorific value varied only about 14 “/o seasonally (on a dry-weight basis). This suggests

a marked

seasonal

variation

in calorific

value

of live material

but,

contrary to our results, with highest calorific value/g live material in June and lowest value in December (no autumn data given). If the same were true of L. longicruris in Newfoundland, then the caloric intake of Strongylocentrotus droebachiensis would have been very low in the winter and very high in the spring in the 1969 study referred to above. This is essentially what Miller & Mann (1973) found in their studies on the seasonal aspects of the energy budget of S. droebachiensis on a diet of Laminaria longicruris in the St Margaret’s Bay area. Their study indicated that a 40 g urchin about 47 mm in diameter would take in 0.22 kcal daily in FebruaryMarch and 0.60 kcal daily in June-July.

SEASONAL FOOD PREFERENCES

CHANGES

AND RELATED

IN CALORIFIC

VALUE

OF

SEAWEEDS

149

FACTORS

There are two ways to measure the food preference of an animal: 1) determine the chemosensory, tactile, or visual attractiveness of a food (information used by an animal

to locate,

or 2) record

and to select, one food over another

the amount

of one

in choice experiments),

food which is eaten as compared

with another,

when both (or several) are offered simultaneously. Many workers have used experimental designs of the second category to determine food preferences of invertebrate herbivores (e.g., Carefoot, 1967; Leighton, 1966; Leighton & Boolootian, 1963). In our study of Kutherina the attractiveness of the foods and consumption rates were measured separately. In the former type of experiment we found that Hedophyllum was chosen over Zriduea 75 “/:, of the time. Strictly on the basis of caloric content it would have been advantageous for Kutherinu to choose Zridueu, but other factors are involved; e.g., in July 1972 Kutherinu only ate about 0.4 live g of Zridueu daily, providing 0.24 kcal, whereas the animals ate about 1.2 live g of HedophJJlum daily, providing 0.4 kcal. Here, feeding preference may be correlated not with the calorific value of the food, but with the amount of food that is eaten. In the cases of Iridueu and Hedophyllum, shape and texture may be important in determining the rate at which Kutherina can eat them. The three-pronged radular teeth of Kutherinu are long, sharp, and slightly concave and this shape may be more effective for chiseling pieces from a thick fleshy alga like Hedophyllum than from more limp material like Zridueu. Vadas (1968) and Paine & Vadas (I 969) discussed food preference and calorific value of algae eaten by invertebrate herbivores from their own and other data in the literature. It should be noted that they used the term “preference” for the most part to apply to the greater amount of one alga eaten over another when the animal was given a choice, but it was also applied to situations involving the purely chemosensory attractiveness of one alga over another (Vadas’ 1968 food preference experiment

No. 2), and to data from single-diet

feeding experiments

where one alga

was eaten at a greater rate than another (Fuji’s 1962 data; Vadas’ 1968 food preference experiment No. 4). While we do not agree that a preference can be measured by the latter method, it is nonetheless clear from these studies that calorific values and food preferences do not correlate for a number of invertebrate herbivores; in several instances the most energy-rich foods were the least preferred. Calorific value is, however, only one of many factors which may have been involved in the evolution of attractiveness of various foods to an animal. Indeed, if calorific value were the only criterion it would be expected that all animals in a given habitat would prefer the single most energy-rich food. In the Kutherinu example above, an important factor appears to be the rate at which a food is eaten - the greater the rate, the greater the intake of calories and other nutritional components. In Vadas’ (1968) food preference experiment No. 2 the brown algae, Laminuria saccharina, Nereocystis luetkeanu, Costariu costuta, Agarwn crihrosum, and A. jim-

JOHN H. HIMMELMAN

150

briatum

value,

(those

species for which comparable

food preference,

in accordance droebachiensis,

examine behaviour

AND

feeding

THOMAS

H. CAREFOOT

data are given by Vadas

rate, and assimilation

efficiency)

on calorific

are ranked

solely

with their sensory attractiveness to the sea urchins, Strongylocentrotus S. franciscanus, and S. purpuratus. With these data we may now

the hypothesis

that

the above

which causes them to choose

sea urchins

may have evolved

a sensory

foods which they can most readily eat and

assimilate. Although Vadas found no correlation between the sensory attractiveness of a food to the urchins and its calorific value, his data do show that there is better correlation of preference (sensory attractiveness) with the rate at which the algae were eaten (but being statistically significant only for S. franciscanus; Spearman Rank Correlation Coefficient Analysis; P < 0.05). Furthermore, when the caloric intake is calculated, there are statistically significant correlations with food preferences for S. droebachiensis and S. franciscanus. This is also true when assimilation efficiency is taken into consideration, and for S. ,franciscanus food preference and the number of calories absorbed show excellent correlation for the five diets. None of the above correlations were statistically significant for S. purpuratus. It was clear that the Agarum spp. were least preferred by StronglJocentrotus purpuratus and provided the least number of calories when eaten as compared with the three other plant species, but this sea urchin species preferred Laminaria saccharina and Nereocystis luetkeana over Costaria costata even though the calculated caloric intake indicated that Costariu would be a better food. This anomaly could be explained by the greater availability of Laminaria and Nereocystis to Strongylocentrotus purpuratus which is a relatively sedentary urchin and relies to a large extent on food carried to it by waves and currents. Laminaria and Nereocystis, being more abundant than Costaria might be more readily available to the urchins giving rise to the evolution of a preference for these seaweeds over Costaria. In summary, on an a priori expectation, an animal’s dietary preference should be positively correlated with those foods from which it can derive the greatest benefit. The calorific value of a food, although an important nutritional component, would not be expected necessarily to correlate with food preference. Other factors are also important.

The feeding apparatus

may be effective in manipulating

some foods, but

clumsy with regard to other foods, hence, determining feeding rate. An animal may not have the necessary enzymes to digest some materials, and the rates of absorption of different foodstuffs will vary; some foods may provide greater quantities of necessary vitamins, amino acids or mineral substances (Carefoot, 1973). In addition to these nutritional factors, it would have been of advantage to an animal to have evolved an ability to locate, eat, and digest foods which are readily available in its habitat (Paine & Vadas, 1969). The relative effects of these factors will vary from situation to situation and no one factor or combination of factors will be consistently important in determining the food preference of an animal.

SEASONAL

CHANGES

IN CALORIFIC

VALUE

OF SEAWEEDS

151

ACKNOWLEDGEMENTS

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