Tane (1968) lh: 25-k2 25

THE FEEDING BEHAVIOUR OF ROSTANGA RUBICUNDA (MOLLUSCA, NUDIBRANCHIA).

By A. M. Ayling*

INTRODUCTION

Most members of the order Nudibranchia are spec­i a l i s e d carnivores feeding on s e s s i l e and encrusting animals such as hydroids, polyzoans, P o r i f e r a , ascldians and alcyonarians. A l l have d i f f e r e n t means of feeding eg. sc r a p i n g , t e a r i n g or sucking and d i f f e r ­ent m o d i f i c a t i o n s e s p e c i a l l y i n the buccal mass. The l e a s t s p e c i a l i s e d of these grazing carnivores are the members of the Doridacea which feed on sponges. Most are b r i g h t l y coloured e i t h e r f o r camouflage when on the food sponge or to serve as a warning f o r predat­ors. The b r i g h t red Rostanga rufescens of B r i t a i n feeds on the encrusting red sponge Microciona i n the order P o e c i l o s c l e r i d a (Morton) and the very s i m i l a r R. pulchra (MacFarland) of North America feeds on a sponge of the same order Ophlitaspongia penata (Cook 1962). The New Zealand species R. rubicunda (Cheeseman) occurs commonly on Westmere r e e f , Auckland, i n a s s o c i a t i o n w i t h three very s i m i l a r sponges.

Microciona coccinea Holoplocamium neozelanicum Ophlitaspongia seriata

The feeding of R. rubicunda i n r e l a t i o n to these three sponges was i n v e s t i g a t e d using a number of techniques.

The food of carnivores and scavengers i s fr e q u ­e n t l y l o c a l and s p e c i f i c and thus chemoreception from a distance i s undoubtedly important i n feeding behav­i o u r . R. pulchra i s a t t r a c t e d to Ophlitaspongia pennata by chemotaxis (Cook 1962) and i t was thought that the same was probably true of the r e l a t i o n s h i p between R. rubicunda and one or more of the above ^Department of Zoology, University of Auckland.

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mentioned sponges. The small s i z e of t h i s d o r i d and i t s ease of c o l l e c t i o n make i t p o s s i b l e to attempt the type of feeding behaviour experiments used by Stehouwer (1952), Braams and Geelen (1953) and Cook (1962) to determine i t s food preferences and other aspects of i t s feeding behaviour. This method was sub s t a n t i a t e d by making s p i c u l e mounts of gut contents and faeces t o determine the sponges eaten and als o by observing the animal i n the f i e l d .

FIG. 1. ROSTANGA RUBICUNDA.

EXTERNAL CHARACTERS

Rostanga rubicunda (Cheeseman l 8 8 l ) i s a small b r i g h t s c a r l e t nudibranch that seems to be very close to the B r i t i s h R. rufescens and the North American R. pulchra, MacFarland. The mantle i s covered with minute, c l o s e l y packed, erect tubercules and the foot

27

extends a short distance p o s t e r i o r l y t o t h i s . The rhinophores are completely r e t r a c t a b l e and have 12 broad laminae which run o b l i q u e l y upwards. The apex i s a small p r o j e c t i n g f l a t topped s t y l e . The r h i n o ­phores of nudibranchs were developed f o l l o w i n g the los s of c t e n i d i a and the osphradium as a replacement sensory area and are clubbed and f i n e l y p l i c a t e to increase the sensory epithelium. They contain r e l a t ­i v e l y l a r g e lobed g a n g l i a associated w i t h the recep­t o r s . In Rostanga the rhinophores seem t o be used f o r d e t e c t i n g the presence of the food sponge at a distance i e . by chemotaxis (Cook 1962) although Augersberg (1922) a f t e r experiments with food e x t r a c ­t s concluded that the rhinophores were not inv o l v e d w i t h chemoreception at a dist a n c e . However, placed as they are i n an a n t e r i o r , elevated p o s i t i o n i t would be f a i r to suggest that the f u n c t i o n of the rhinophores i s s i m i l a r to that of the osphradium they replace i e . t o t e s t the water f l o w i n g over them f o r contained chemicals, e i t h e r favourable (food) or un­favourable. The g i l l s (branchiae) are a l s o r e t r a c t ­a b l e , eight i n number, erect and b i p i n n a t e .

ECOLOGY

Rostanga rubicunda can be found o c c a s i o n a l l y i n the s u b l i t t o r a l f r i n g e on most protected rocky shores i n the North Auckland area, eg. Eastern beach, Waiwera, Takapuna, Bonaccord harbour, Leigh. I t i s , however, l i m i t e d i n numbers i n most of these areas by the s c a r c i t y of i t s food. But on Westmere reef which straddles the main t i d a l stream of Auckland Harbour the d e t r i t u s r i c h waters which surge twice d a i l y across i t provide ample nourishment f o r a p r o l i f i c growth of sponges. The three food sponges of Rostan­ga rubicunda occur q u i t e commonly amongst these and t h i s s l u g occurs i n considerable numbers at t h i s l o ­c a l i t y . In t h i s area the slugs are not found as part of the under-stone fauna but p r e f e r more open s i t u a ­t i o n s even though t h e i r food sponges are often pres­ent under stones. Approximately 50% of the Rostanga population were found feeding on the red food sponges. The sponges eaten by 20 of these feeding slugs were

28

i d e n t i f i e d using s p i c u l e mounts. I I were feeding on Ophlitaspongia 7 " " " Microciona 2 " " " Holoplocamium

Rostanga was found i n considerable numbers over the e n t i r e p e r i o d during which they were examined, i e . from e a r l y March t o September. Powell (1957) s t a t e s that i t a l s o occurs commonly over the months September t o November. Thus i t i s probable t h a t t h i s animal may be found throughout the year w i t h equal abundance. The smallest slugs c o l l e c t e d were about 10 mms. i n length and the l a r g e s t 33 mms. with an average of 15-20 mms.

FEEDING BEHAVIOUR

M a t e r i a l s and Methods Rostanga rubicunda3 as has been pointed out, i s

always found where i t s food sponges are present and as sponges occur i n regions where there i s consider­able water movement i t should be p o s s i b l e f o r the animal t o t r a c e i t s food by det e c t i n g s e c r e t i o n s from the sponge and f o l l o w i n g them through the current t o t h e i r source, i e . by chemotaxis. As Rostanga feeds on at l e a s t three sponges the response t o each sponge would be expected to increase w i t h the slugs' p r e f e r ­ence f o r t h a t sponge as food. To t e s t t h i s an a r t i ­f i c i a l current flow was set up i n the la b o r a t o r y and arranged so th a t the slugs could be given a choice between two sponges. To achieve t h i s seawater was run i n t o two bowls i n which the various sponges could be placed and then siphoned out i n t o a s i n g l e shallow t r a y i n which the slugs to be t e s t e d were placed. The water was allowed to overflow from the t r a y and run to waste as i t could not be r e c i r c u l a t e d without mixing the sponge "odours". The apparatus use i s shown i n F i g . 6, and d i a g r a m a t i c a l l y i n F i g . 2.

( i ) Using t h i s apparatus f i v e f a i r l y s i m i l a r sponges from Westmere were t e s t e d against blank c o n t r o l s and against each other to f i n d out which were eaten by Rostanga and the order of preference

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MCOMINO 5CAWATER

SLUG TRAY

' l i l t O V F » F L O W

* INFLOW

FIG. 2. CURRENT FLOW APPARATUS.

amongst these.

These sponges were: -Ophlitaspongia seriata Holoplocamium neozelanicum Microciona coccinea Hymeniacidon perleve Suberites cupuloides

Other aspects of Rostanga's feeding behaviour were t e s t e d using t h i s apparatus, v i z . ( i i ) Gregariousness - a few of the slugs themselves

were placed i n one of the sponge howls to see the slugs i n the t r a y were a f f e c t e d at a l l .

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( i i i ) The " f o u l i n g " e f f e c t s of other encrusting org­anisms and algae found a s s o c i a t e d w i t h the sponges on the r e a c t i o n of the slugs was i n v e s ­t i g a t e d t o see i f the presence of s e c r e t i o n s from other organisms masked those from the sponge and confused the s l u g s ' sensory mechan­isms.

( i v ) The e f f e c t s of v a r y i n g the current speed were t e s t e d by r e g u l a t i n g the siphoning height be­tween the bowls and the t r a y .

(v) The e f f e c t s of l i g h t or dark On the s l u g s ' r e a c t i o n s were t e s t e d to see i f feeding a c t i v ­i t y was g r e a t e r during the day than at night or v i c e versa.

( v i ) The minimum amount of sponge needed to give a d e f i n i t e r e a c t i o n was i n v e s t i g a t e d .

To see i f the slugs could detect the sponges without water movement another apparatus was set up i n which the sponge se c r e t i o n s could only reach the slugs by d i f f u s i o n . In t h i s the two sponge bowls were placed at e i t h e r end of the t r a y c o n t a i n i n g the s l u g s ; the three l i n k e d by water bridges. These bridges were made as short as p o s s i b l e t o minimise the d i f f u s i o n path (see F i g . 3. ). A f t e r f i v e 3 hr. experiments using sponges t h a t evoked a considerable r e a c t i o n i n the current flow apparatus and 35 s p e c i ­mens of Rostanga i n the t r a y none of the animals had responded. I t i s thus probable that water movement i s necessary t o enable Rostanga to detect and seek out i t s food.

Results Each experiment was run f o r three hours and at

the end of that time the animals i n each sponge bowl were counted. The number of animals remaining i n each tube was a l s o noted and both f i g u r e s recorded as percentages. The slugs were removed from the bowls as soon as they reached them t o prevent feeding on the sponges.

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* — z ^ T ^ SIPHON

S P O N G E BOWL

SPONGE • O W L

FIG. 3. DIFFUSION APPARATUS

Table 1.

Controls

Run no. Bowl Contents of bowl % i n bowl %in tube

I. A. n i l 2. 7 0 B n i l 1. 1+ 0

2 A n i l 0 0 B n i l 0 0

Feeding preference experiments

3 A n i l 0 1. 1+ B l+. 55gm. Ophlitaspongia 26 13. 7

1+ A l+. 55gm. Ophlitaspongia 31. 5 5-5 B n i l 0 0

5 A 2. 25gm. Ophlitaspongia 20. 6 l+. l B 2. 3gm. Ophlitaspongia 15-1 9. 6

6 A n i l 1. 1+ 1. 1+ B lgm. Holoplocamium 6. 9

7 A 3-71gm. Holoplocamium 2. fk 6. 9 B n i l 0 1. 1+

Feeding preference experiments.

Gregariousness

" F o u l i n g " e f f e c t s

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(Table 1. continued)

Run no. Bowl Contents of bowl % i n bowl % i n tube

"Fo u l i n g " e f f e c t s

22 b Microciona 23. 3 10

V a r i a t i o n of current speed

23 A Microciona w i t h current v e l o c i t y of 0. 86 m. p. h.

0 0

B Microciona w i t h current v e l o c i t y of O. 58 m. p. h.

26 10

2k A Microciona w i t h current v e l o c i t y of 0. 75 m. p. h.

3 5

B Microciona w i t h current v e l o c i t y of 0. 58 m. p. h.

25 8

25 A Microciona w i t h current v e l o c i t y of 0. 7 m. p. h.

27 3

B Microciona w i t h current v e l o c i t y of O. 58 m. p. h.

7 1

Standardisation of r e s u l t s ( f o r current speed). As they stand the r e s u l t s show comparisons be­

tween only two of the current v e l o c i t i e s at a time and i n order t o compare a l l four v e l o c i t i e s d i r e c t l y they are standardised against one value i e . O. 58 m. p. h. i n run 2k. For example: - A current of 0. 58 m. p. h. i n run 25 was compared with 0. 7 m. p. h. - 7 slugs responded t o 0. 58 m. p. h. and 27 t o 0. 7 m. p. h. I f , however, 25 animals had responded to 0. 58 m. p. h. as i n run 2k then 96 would have chosen 0. 7 m. p. h. etc.

Table 2.

Current v e l o c i t y (m. p. h. ) O. 58 0. 7 0. 75 0. 86

Run 23 26 - - 0 Run 2k 25 - 3 -Run 25 7 27 - -

(Table 2. continued)

Current v e l o c i t y (m. p h. ) 0. 58 0. 7 0. 75 0. 86

S t a n d a r d i s a t i o n 25 96 3 0

See accompanying graph of r e s u l t s ( F i g . k).

CURRENT VELOCITY (M. PH. )

FIG. 4. CURRENT VARIATION

Table 3.

L i g h t and dark

Run no. Bowl Contents of bowl % i n bowl % i n tube

26 A Microciona 8 16 ( c o n d i t i o n s : - l i g h t ]

B n i l 0 0 27 A n i l 0 0

B Microciona 8 10 ( c o n d i t i o n s : - dark)

Minimum amount of sponge 28 A n i l 3. 3 0

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(Table 3. continued)

Run no. Bowl Contents of bowl % i n bowl % i n tube

28 B 0. 37gm Ophlitaspongia 30 21. 7 29 A 0. 2Ugm Ophlitaspongia 11. 7 18. 3

B n i l 0 3. 3 30 A 0. 13gm Ophlitaspongia 5 16. 7

B n i l 1. 6 0 31 A n i l 0 3. 3

B 0. 06gm Ophlitaspongia 3. 3 10

See accompanying graph of r e s u l t s ( F i g . 5).

1 L 1 I

01 0-2 0-3 0 4

WEIGHT O F S P O N G E IN BOWL (GMS. )

FIG 5 VARIATION OF SPONGE WEIGHT,

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F i g . 6. This i s a drawing (taken from a photograph) of the current flow apparatus. The two sponge howls are on the r i g h t and the shallow s l u g t r a y on the l e f t .

Run 12 was i n progress and had been running f o r about 60 minutes w i t h Holoplocamium i n bowl A and Ophlitaspongia i n bowl B. 15-20 slugs are c l u s t e r e d around the entrance t o tube B and k can be seen mov­ing up i t , (arrowed). In contrast to t h i s only a few animals are i n the v i c i n i t y of tube A, and none i n i t . This i s a v i v i d demonstration of Rostanga's a b i l i t y to detect and d i f f e r e n t i a t e between the very s i m i l a r sponges on which i t feeds.

DISCUSSION

( i ) Feeding Preferences Runs 1 and 2 were c o n t r o l s with no sponge i n

e i t h e r bowl. These runs ensured that any r e a c t i o n

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from the slugs i n the experiments was caused by the sponge being t e s t e d and was not a p o s i t i v e r e a c t i o n to the current. As can be seen from the r e s u l t s the number of animals reaching the bowls i s very small i n 1, p o s s i b l y due to random movement of the slugs about the t r a y , and n i l i n 2, i n d i c a t i n g that Rostanga does not show p o s i t i v e r h e o t a x i s .

Runs 3, h and 5 using Ophlitaspongia seriata i n e i t h e r bowl and then i n both bowls show that Rostanga can detect t h i s sponge by chemotaxis. These r e s u l t s a l s o i n d i c a t e that the slugs show l i t t l e or no pre­ference f o r e i t h e r of the two bowls used. This i s important i f comparisons are t o be made w i t h two d i f f e r e n t sponges i n the bowls.

Holoplocamium neozelanicum: - In runs 6 and 7 t h i s sponge also evokes a r e a c t i o n from the slugs but the numbers eg. 12. k% and 9. 6% as opposed to 31% and 39% i n d i c a t e that Ophlitaspongia i s more e a s i l y detected and hence probably p r e f e r r e d as food.

In runs 8 and 9, Microciona coccinea was used and the r e a c t i o n - 1+9-2 and 57• 5% - was greater than e i t h e r Ophlitaspongia or Holoplocamium.

Thus Rostanga appears to feed on a l l three of the P o e c i l o s c l e r i d sponges mentioned and the order of preference which has been deduced from the magni­tude of response may be put at: -

Holoplocamium Ophlitaspongia Microciona

i n c r e a s i n g preference •

Runs 10 and 11 i n v o l v e Hymeniacidon perleve and Suberites cupuloides r e s p e c t i v e l y and the slugs showed no r e a c t i o n t o e i t h e r of these sponges which although somewhat s i m i l a r to the others i n e x t e r n a l appearance belong to d i f f e r e n t orders.

In runs 12 and 13 the responses to Ophlitaspon­gia and Holoplocamium were compared by p u t t i n g one i n t r a y A and the other i n t r a y B. As can be seen

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from the r e s u l t s Holoplocamium, the l e a s t p r e f e r r e d sponge was almost completely ignored i n the presence of the more powerful stimulus from Ophlitaspongia.

Runs lk, 15 l 6 and IT are comparisons between Ophlitaspongia and Microciona. Microciona i s p r e f e r ­red but the d i f f e r e n c e between these two sponges i s not as great as between Ophlitaspongia and Holoplo­camium.

Thus the order of preference put forward on the b a s i s of runs 3 and 9 i s borne out by these f u r t h e r t r i a l s and i t i s a l s o e s t a b l i s h e d t h a t there i s a greater d i f f e r e n c e i n response between Holoplocamium and Ophlitaspongia than between Ophlitaspongia and Microciona.

i e . Holoplocamium—* Ophlitaspongia—• Microciona

i n c r e a s i n g preference

Gut contents and faeces were examined from a number of animals c o l l e c t e d i n t h e i r n a t u r a l h a b i t a t and s p i c u l e mounts made to determine which sponges had been eaten. S p i c u l e s from a l l three of the p o e c i l o s c l e r i d sponges used i n the experiment were found i n d i c a t i n g t h a t Rostanga does indeed feed upon these three sponges.

( i i ) Gregariousness In runs 19 to 21 f i v e Rostanga were placed i n

one of the sponge bowls and nothing i n the other t o see i f the slugs remaining i n the t r a y were a t t r a c t e d to t h e i r f e l l o w s . In two cases there was no response, i n d i c a t i n g t h a t the presence of animals i n the tube or sponge bowl during the experiments was not an a t t r a c t i n g f a c t o r to the slugs s t i l l i n the t r a y and d i d not a f f e c t the r e s u l t s . In the f i e l d t h i s would mean that slugs already feeding on a piece of sponge do not a t t r a c t other animals to them. I t i s p o s s i b l e however, t h a t the damage done t o a sponge during the feeding process would release a greater amount of the a t t r a c t i n g substances i n t o the water and thus f a c i l i t a t e d e t e c t i o n by other slugs. Thus when

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the slugs are found a c t i v e l y feeding on a piece of sponge on the shore there i s oft e n more than one i n ­d i v i d u a l present and o c c a s i o n a l l y up to f i v e . In the other run, three of the slugs crawled down the tube to the main t r a y thus e x h i b i t i n g a negative rheotaxis (response to c u r r e n t ) . This was al s o i n d i c a t e d when the sponge was taken out of the t r a y s at the end of a run when slugs were s t i l l a c t i v e l y crawling up the tube. Many of these reversed d i r e c t i o n when the stimulus was removed and made t h e i r way back t o the t r a y .

( i i i ) 'Fouling' E f f e c t s In run 22, Microciona was placed i n both t r a y s

but i n one i t was associated w i t h other organisms commonly found at Westmere Reef. eg. Sargassum undulatum

Sargassum serratifolium Codium adhaerens Watersipora subovoidea A simple a s c i d i a n

The very close r e s u l t s f o r both t r a y s show that these organisms d i d not a f f e c t the slugs' response to the sponge. Thus the animals would be able t o detect t h e i r food i n t h e i r n a t u r a l h a b i t a t where the sponges are growing amidst a prof u s i o n of these other organ­isms.

( i v ) V a r i a t i o n of current speed Four d i f f e r e n t current speeds were compared

(runs 23 to 25); the r e s u l t s standardised against one value and graphed. The graph shows that there i s an optimum current flow which e l i c i t s the greatest r e s ­ponse from the animals. There are two p o s s i b i l i t i e s to e x p l a i n the f a l l i n response above the optimum current flow: -1. I t i s p o s s i b l e that the sponge se c r e t i o n s would be too d i l u t e d t o permit easy d e t e c t i o n e s p e c i a l l y i n the presence of the more powerful stimulus i n the lower v e l o c i t y current. 2. The slugs may have a negative response t o the

ho

higher current v e l o c i t i e s . The f a l l below the o p t i ­mum i s more d i f f i c u l t t o e x p l a i n but could be due to nonmaintenance of d i r e c t i o n a l flow i n the t r a y , from the low v e l o c i t y tube. Thus, although the s e c r e t i o n s from the low v e l o c i t y tube were more concentrated the slugs ignored them i n favour of the stronger current which could be t r a c e d more e a s i l y .

(v) E f f e c t s of Light and Dark In run 26 , (Table 3 ) , Microciona was placed i n one

bowl and k x 100 watt bulbs w i t h r e f l e c t o r s placed 3 f t above the apparatus to provide an intense source of l i g h t . In run 27, Microciona was placed i n the bowl and the experiment l e f t i n darkness. The r e s ­ponse was s i m i l a r i n both cases i n d i c a t i n g that Rostanga probably detects i t s food and feeds e q u a l l y e f f i c i e n t l y regardless of whether i t i s day or n i g h t .

( v i ) Minimum amount of Sponge Four runs were made (runs 28 to 31) using s t e a d i l y

decreasing weights of Ophlitaspongia. The r e s u l t s show that the slugs could respond t o a piece as small as 0. 06gm, i e . a 2mm cube of sponge and t h i s at a distance of 52cm w i t h a current flow of O. 58 m. p. h. The graph of response against weight (graph 2) shows that an increase i n the weight of sponge leads t o a steady increase i n response p o s s i b l y due t o d i f f e r ­ences i n the i n d i v i d u a l s e n s i t i v i t y of the animals to the sponge s e c r e t i o n s . In the f i e l d where the m a j o r i t y of the sponge masses are very much l a r g e r than 0. 06gm most sponges i n an area would be open to d e t e c t i o n and thus feeding by Rostanga and s i z e of a sponge does not l i m i t i t s a v a i l a b i l i t y .

SUMMARY

1. Rostanga rubicunda feeds on three very s i m i l a r sponges i n the order P o e c i l o s c l e r i d a and can det­ect and then l o c a t e these by chemotaxis. Rostanga shows d e f i n i t e preferences amongst these, p r e f e r r ­ing Ophlitaspongia seriata to Holoplocamium neoze-lanicum and p r e f e r r i n g Microciona coccinea to both

1+1

of these. 2. Rostanga responds t o very small concentrations

of the s t i m u l a t i n g substances and located a piece of sponge 0. 06gms i n weight at a distance of 52cm.

3. Rostanga does not show gregariousness and the slugs are not a t t r a c t e d t o each other during feeding a c t i v i t i e s .

k. Rostanga could d i s t i n g u i s h the sponge s e c r e t i o n s amongst those from the encrusting animals and algae, i e . i n the type of s i t u a t i o n encountered i n t h e i r n a t u r a l h a b i t a t .

5. There i s an optimum current v e l o c i t y at which Rostanga shows a maximum response to the sponges.

6. Rostanga shows equal feeding a c t i v i t y both day and night.

REFERENCES

Morton J . E. 1967 -+th. ed. Molluscs Hutchinson. Cook E. F. 1962 Food choices of Rostanga pulchra

and Archidoris. Veliger, 4 (U). Braams W. G. and Geelen H. F. M. 1953 Preferences of some nudibranchs f o r c e r t a i n c oelenterates. Arch­ives Neerlandaises de Zoologie 10 (3) .

Stehouwer H. 1952 Preferences of Aeolidia p a p i l l o s a f o r the sea anemone Metridium senile. Archives Neerlandaises de Zoologie 10.

F o r r e s t J . E. 1953 Dorid feeding. Proc. Linn. Soc. Land. 164.

Powell A. W. B. 1961 1+th ed. S h e l l s of N. Z. Whitcom-be and Tombes.

Suter H. 1913. Manual of N. Z. Mollusca. Government P r i n t e r s (Wellington).

Augersburg 1922. Chemical and p h y s i c a l s t i m u l a t i o n of rhinophores. J. Expl. Zool. 29.

M i l l e r M. C. 1 9 6 l . D i s t r i b u t i o n and food of nudi­branchs of the I s l e of Man. J. Anim. Ecol. SO.

1+2

Wilber K. and Yonge CM. 196U & 1966 Physiology of the M o l l u s c a V o l . 1 and 2. Academic Press.