Function of the gizzard in Bryozoa

J. Exp. Mar. Biol. Ecol., 1987, Vol. 107, pp. 21-37

21

Elsevier

JEM 00841

Function of the gizzard in Bryozoa J.B. Markham

and J. S. Ryland

Department of Zoology. University College of Swansea, Swansea, Wales

(Received 20 October 1986; revision received 24 November 1986; accepted 8 December 1986) Abstract: The gizzard, a modified region of the stomach cardia incorporating chitinized teeth or plates

surrounded by circular muscle, has been reported in 16 bryozoan genera (one Cheilostomata, 12 Ctenostomata, three Cyclostomata) and has independently evolved at least six times. Its occurrence is reviewed in the light of revised taxonomy of stolonate ctenostomes. The ability to crush diatom frustules and to separate valves intact has been investigated in bryozoans with (Bowerbankia spp., Amathia pruvoti Calvet) and without [Electra pilosa (L.) and Fh4streZZidra hispida (Fabricius)] a gizzard. The gizzard-bearers have significantly greater ability to break the frustules, except for Amathia pruvoti in comparison with Flustrellidra hispida. F. hkpida and Electra pilosa have good ability to open frustules of some diatoms, even to the extent of equalling the percentage broken by the gizzard of Bowerbankia. These findings have been related to the size of the lophophore and mouth in bryozoans, and to the size of the diatoms. Notwithstanding the recently recognized profusion of nanoplanktonic diatoms, a majority of the common species are large, often too large to be ingested by the characteristically small bryozoans that possess a gizzard. This paradox is discussed in the context of gut function, habitat, and possible specialization by the bryozoans to exploit different food resources. Key words: Bryozoa; Gizzard; Function of gut; Food resource

The objective of this study was to determine whether the presence of a gizzard in a bryozoan increases its ability to crush or open diatom frustules. This might provide insight into the extent to which marine Bryozoa are specialized to exploit different food resources. The literature on bryozoan gizzards has been briefly discussed from limited but different viewpoints by Jebram (1973), Gordon (1975a), Ryland (1976), Winston (1977), and Schafer (1986b). Only a few of ~~4000 species of living Bryozoa possess what is generally termed a gizzard. They belong to 16 genera (see Table VII) (although these are not the same 16 as in the recent tabulation by Schafer, 1986b), mainly from the order Ctenostomata, especially from the Vesicularioidea in which the gizzard is diagnostic. The exceptions are the cheilostome genus Plesiothoa (Gordon & Hastings, 1979) and probably three genera of Cyclostomata (Boardman & McKinney, 1986; Schafer, 1986a,b). It seems that a gizzard must have independently evolved in Bryozoa at least six times. Correspondence address: J. S. Ryland, Department of Zoology, University College of Swansea, Swansea SA2 8PP, Wales 0022-0981/87/$03.50 0 1987 Elsevier Science Publishers B.V. (Biomedical Division)

22

J.B. MARKHAM AND J.S. RYLAND

The anterior gut (pharynx or oesopha~s) of Bryozoa has no digestive function (Silen, 1944). The stomach, which has secretory and absorptive walls, is differentiated into three regions : cardia, caecum (which is sac-like) and pylorus, and precedes the posterior gut (rectum). In the Victorellidae there is normally no gizzard but the cardia incorporates an annular sphincter muscle (quite distinct from the oesophageal-cardiac valve). The sphincter may be more or less central in the cardia, as in F%toreZia(~n~d~e, 1916), or adjacent to the caecum, as in Tanganella (Braem, 195 1). The pre-sphinctal chamber may be slightly chitinized and was believed by Annandale to act as a store for hard particles, particularly diatoms, which he thought might damage the caecum. Interestingly, Jebram (1982b) has observed that the sphincter itself crushes cells as they pass into the caecum. The sphincter of 3ul~lla, situated midway as in Victorella, may incorporate small teeth in European material (Braem, 1951), although these have not been detected in material from North America (Jebram & Ever&t, 1982). It has been stated that a cardiac chamber is also present in Nolella (Harmer, 1915) and certainly both Harmer’s illustration of N. papuensis (Pl. IV, Fig. 19) and Calvet’s (1900) of N. dilatata show a cardia with bulges and constrictions. There is, however, no indication of any sphincter in a detailed lon~tu~n~ section (Calvet, 1900, Pi. VII, Fig. 12). The cardia in the freshwater genus Hislopiu has three regions, the central one being enlarged and globular, with a smooth horny lining. According to Annandale (1916), it has no crushing function and acts as a store, although it is often termed a gizzard in the literature. Its covering of circular muscle suggests an origin from a sphincter positioned as in Tanganel~a or Victoretla, although recent classifications (Jebram, 1973, 1986; d’Hondt, 1983) do not support close relationship. An unusual feature is a ciliated annulus between this proventriculus and the caecum. The most familiar and best studied gizzard is found in the Vesicularioidea, e.g. Bowerbankia spp. (Braem, 195 1; Bobin & Prenant, 1952; Brien, 1960; Gordon, 1975b), Spath~ora comma (Bobin & Prenant, 1954), and Z~~~n ~e~iciila~m (Ries, 1936; Cori, 1941). It is spherical and adjacent to the caecum. Its wall incorporates circular muscle, thickest equatorially, implying an origin via a sphincter sited as in Tunganella (Jebram, 1973) although the Vesicularioidea are not believed to be closely related to the Victorellidae (but see Jebram, 1986). The lining epithelium is produced into rows of jagged teeth, each tooth the product of a single cell. The teeth are arranged in groups of two different sizes and degrees of hardness (Bobin & Prenant, 1952, 1954) and are structurally similar to other epidermal derivatives known as “annelid-like” setae (Gordon, 1975b). The cheilostome PZesiothoa(formerly Hippothoa pro parte), also has small unicellular teeth lining the gizzard, although they are fewer and rounded (Gordon, 1975a). This gizzard is also s~ounded by circular muscle. The remaining gizzards incorporate an arrangement of two or four flat plates of multicellular origin. That of CryptopoZyzoonhas an opposing pair of such plates, and the wall includes a thick muscular annulus (Dendy, 1888; Waters, 1910; Marcus, 1941). The recently discovered gizzard in Cyclostomata also has two plates (Boardman 8z

FUN~IONOFTHEGIZZARDINBRYOZOANS

23

McKinney, 1986; Schafer, 1986a) and has been described in detail by Schafer (1986b). In Annectocyma (“Diaperoecia”), at least, the plates are hinged. The gizzard ofAeverrillia has four plates (Osbum & Veth, 1922, as Buskia; Marcus, 1941; Rogick, 1945). Digestion in Bryozoa is both extra- and intracellular, with the caecum being the primary site of both (Ries, 1936). Very small diatoms may be ingested whole by these cells (Gordon, 197%). The pylorus typically is ciliated in Gyrrmolaemata and Stenolaemata, and its contents, including a compacted cord of particles (the ergatula of Morton, 1960), are rotated at, e.g., 70-150 rpm in ~embrani~ru (Silen, 1944). Species of ctenostomes which have a gizzard reportedly lack this rotating cord (a fact we confirm for Bower~nkia citrina and B. ~mbn~ata), perhaps because the gizzard makes this type of breakdown and digestion unnecessary (Silen, 1944), although published illustrations show a ciliated pylorus in Bowerbankia (Braem, 1951; Brien, 1960), Bulbella (Braem, 1951), Cryptopolyzoon (Dendy, 1888; Marcus, 1941) and Zoobotryon (Ries, 1936; Cori, 1941). Our observations, however, suggest that very occasionally there is some rotation of unconsolidated particles in the stomach of Bowerbankia imbricata. A ciliated pylorus also occurs in the cyclostome Annectocyma although the thick calcified walls of the zooid, of course, preclude observation (Schafer, 1986b). Digestive enzymes might cause the valves of diatoms to separate even in the absence of a gizzard, ahhough many are found intact in the faecal pellets of freshwater bryozoans (T. S. Wood, quoted by Ryland, 1975). Bullivant (1968) found that the gizzard-bearing Zoobotryon flourished on a diet of Phaeodactylum, whereas Bugula neritina, which lacks a gizzard, did not. Winston (1977) reviewed the literature relating to the influence of diet on growth and concluded that diatoms probably are suitable foods for bryozoans with gizzards, but not for those without. Jebram (1975), however, found that growth of Bowerbankia gracilis on single-food diets was greater on either the dinoflagellate Oxyrrhis marina or the cryptophycean Cryptomonas sp. than on either of the diatoms Cyclotella nana and Phaeodactylum tricomutum. Even gizzard-bearing species may therefore thrive better on a diet of naked flagellates than exclusively on diatoms. The effectiveness of the lophophore in capturing highly elongate or spiny particles, or diatom chains, is perhaps open to question (Ryland, 1975).

MATERIALS AND METHODS

Bryozoa for the experiments were collected mainly from the Mumbles, near Swansea, the gizzard-bearing Bowerbankia citrina (Hincks), B. gracilis Leidy, B. gracillima (Hincks), and B. imbricata (Adams) from the sheltered vicinity of Mumbles Pier, and the gizzardless Electra pilosa (L.) and Flustrellidra hispida (Fabricius) from the more exposed Bracelet Bay. Amathia pruvoti Calvet, also gizzard-bearing, came from Swanage, Dorset. Each species was cleaned of cont~a~g epibionts, especially entoprocts and other bryozoans. All the gizzard-bearing bryozoans employed had small lophophores (8 or 10 tentacles), as did Electra pilosa (10-15). Fl~trellidra hisp~dahas

24

J.B. MARKHAM

AND J.S. RYLAND

one of the largest lophophores (27-30 tentacles), and was included to check for any ability of a large gizzardless species to deal with diatoms. A literature search was made to establish the number of tentacles and mouth diameter of bryozoans with and without a gizzard. Four diatom species, PfzaeodactyIum tricomuhrm Bohlin, Navicula sp. (LB1050/6), Thal~siosira ~uvia~lis Hustedt, and ~~tzsch~aclusters (E~enberg) W. Smith (LB 1052/8) were selected on account of combined suitable characteristics, viz., small enough to be ingested by experimental bryozoans, few empty (degenerate) fiustules, ability to withstand damage while the faecal pellets containing them were ultrasonically disrupted, and a distinctive frustule shape that could be distinguished from debris, even after crushing. All except P~e~e~l~ ~~omu~rn were obtained directly from the Culture Centre of Algae and Protozoa, Cambridge, and cultured in marine Erdschreiber. P. tricomutum had been in culture at Swansea for some time. Observations were made on the contents of bryozoan faecal pellets to evaluate: (1) the difference in the percentages of P. tricomutum frustules broken during passage through the gut of Electra pilosa and Fl~trell~ra hispida, and the gizzard-bearing Amathia pivot, Bowerbankia citrina, B. gracilis, and 3. ~ac~lima; (2) the difference in the percentages of frustules of Navicula broken by Electrapilosa and Flustrellidrahispida, and by Bowerbankia imbricata; (3) the difference in the percentages of Thalassiosira fruviatilis frnstules broken or with separated unbroken valves after passage through Electra pilosa and Flmtrellidra hispida, and through Bowerbankia gracilis and B. imb~eata; and (4) the Werence in the percentages of broken and separated frustules of Nitzschia cluster&m in Electra pilosa, Fl~~ell~ra hispida, and Bowerbankia imbricata. To clear the gut of possibly confusing debris, each bryozoan was placed in a dilute suspension of the appropriate diatom prior to an experiment. After being allowed to feed and defaecate, each colony was washed clean of faecal pellets (which were discarded). The clean bryozoan colonies were placed in the experimental suspensions of diatoms. The faecal pellets produced were collected by micro-pipette and washed to remove any diatoms that had adhered subsequent to egestion. The pellets were dispersed on a microscope slide using an ultrasonic probe set to an appropriate frequency and amplification determined by pilot experiments. The duration of treatment needed to disperse each batch of pellets was recorded. The slide was systematically scanned under phase and the relative number of frustules or fra~ents contrast at up to x 1000 m~~cation, of fiustules enumerated for each trial. Trials were replicated three to eight times for each diatom-bryozoan combination, except for those involving Phaeodactylum tricomutum where three experimental variants were used. The ability of a bryozoan to open frustules might be influenced either by the extent to which the gut is crammed with food or by the presence of mineral grains. The experimental variants were designed to expose any effects of these factors. Accordingly, the P. t~~ornu~rn suspensions were varied as follows: (l)diluted by x 100 using filtered sea water; (2) diluted by x 100 using Mumbles Pier sea water, which has a large sediment load; (3) diluted by x 10 with Mumbles Pier sea water.

FUNCTIONOFTHEGIZZARDINBRYOZOANS

25

The controls consisted of an appropriate diatom suspension placed on a microscope slide. The volume of this sample and characteristics of its exposure to ultrasonic vibration were identical to those of the corresponding experiment. Six control replicates were compared with each diatom-bryozoan combination; in combinations involving P. tricomutum, one control variant was matched to each of the experimental variants. The controls were scanned and the fiustules assessed as in the experiments. P. tricomutum is not a normal member of the phytoplankton, being found in brackish pools (Lewin, 1958). It is a rather aberrant polymorphic diatom whose planktonic fusiform (cf. benthic oval) phase has a cell wall that consists almost exclusively of organic material (Lewin et al., 1958; Reimann & Volcani, 1967); typical diatoms have a silica-impregnated fi-ustule. The fusiform phase measured up to x25-35 pm in our culture. The oval and triradiate phases were not enumerated. Nuviclrlu sp., z 13-15 x 4.5 pm, has afiustule that is rectangular in girdle view and elliptical in valve view (resembling the species shown in Fig. 168 of Lebour, 1930). Its frustule therefore has four distinct comers, all visible in girdle view, but with only two visible in valve view. Thalassiosiru jluviatilis is a planktonic, estuarine centric diatom, usual diameter 15-23 pm (Hendey, 1964), drum-shaped as in Coscinodiscus. Nitzschiu closterium is an actively mobile pennate diatom, x43-47 x 4.5-7 pm in our culture, spindle-shaped like Phaeodactylum tricomutum, composed of a central body and two apiculate arms. It is found near the shore in slimy dense masses (Hendey, 1964). Unlike P. tricomutum, the valves are silicified and were frequently fractured by the bryozoans along the apical or valvar planes (cf. trans-apical plane: see Boney, 1975). The criteria for enumerating fragmented frustules in four such different species were individually and carefully defined to ensure counts of the greatest accuracy.

RESULTS PHAEODACTYLUM

TRICORNUTUM

The percentage of frustules broken in each experiment was determined. As the differences in the percentages broken in the three control variants for each P. tricomutum - bryozoan combination were small and similar, mean values were calculated for each combination. The appropriate mean was then subtracted from the percentage broken in each of the experimental variants, thereby estimating the percentage of fiustules broken during their passage through each bryozoan’s gut (Table I). The percentages broken were similar in each of the three variants of each P. tricomutum - bryozoan combination. Thus any effect of high cell concentration or high suspended loads was so small that the variants could, in fact, be regarded as replicates. The mean percentage broken was much greater in the gizzard-bearing species (P < 0.05, ANOVA and Dunn-Sidak method of non-orthogonal comparisons among means: Sokal & Rohlf, 1981).

26

J.B. MARKHAM

AND J.S. RYLAND

TABLE I Comparison of the percentage of Phaeodacrylrrm Iricornutum frustules broken during passage through the gut of bryozoans with and without a gizzard: the three experimental variants are defined on p. 24. Percentage broken Variant Species

1

2

3

Mean

43 33 54

9 41 71

24 14 29

25 29 51

51

56

28

45

1

9

-2

3

9

9

-2

5

Gizzard present Amarhia pruvoti Bowerbankia cifrina B. gra& B. ~a~~li~a

Gizzard absent Electra pilosa Flustrellidra hirpida

NA VICULA SP. The percentages broken were calculated as above (Table II). Those for the gizzardbearing B. imbricata were again much greater and non-overlapping with those of either E. pilosa or F. hispida (P < 0.01, ANOVA and Dunn-Sidak method). TABLE II

Comparison of the percentage of Naviculu sp. fiustules broken during passage through the gut of bryozoans with and without a gizzard. Percentage broken Species

Replicate values

Mean

Gizzard present Bowerbankia imbniara

19

19

- 1.1 - 1.1

- 1.1 - 1.1

23

31

33

25

Gizzard absent Electra pilosa FIustrellidra hlspida

THALASSIOSIRA

- 0.6 - 0.9

- 0.9 - 0.9

2.2 - 0.1

0.1 - 0.9

FLUVIATILIS

Percentages broken were calculated as before, as were the percentages of frustules with unbroken, separated valves (Table III). Some unbroken separated valves may have been produced when fiustules were crushed but only one valve broke. Any such effect was assumed ne~~ble. The percentages broken in the guts of gizzard-bearers was again greater (P < 0.01, ANOVA and Dunn-Sidak method: Table IV). The mean percentage of valves separated (PVS) in Flustrellidra hispida was different (P < 0.05) from that in either Bowerbankia gracilis or B. imbricata, as was the difference between Electra pilosa and Bowerbankia gracilis. This ability of Flustrellidra hispida and

27

FUNCTION OF THE GIZZARD IN BRYOZOANS

Electra pilosa to separate valves unbroken was insufficient to negate the advantage of

the gizzard in breaking open frustules because the sum of percentages broken plus separated in either species of Bowerbankia was much greater than in either Electrapilosa or Flu&rellidra hispida (P < 0.01). TABLE HI Comparison of the percentage of l?talassiosira fluviatilis frustules broken or with separated valves after passage through the gut of bryozoans with and without a gizzard: means + SD in parentheses.

Species

Number of replicates

Percentage broken

Percentage separated

Percentage broken or separated

3 5

79.3 (+ 7.6) 84.4 ( f 15.0)

- 4.3 (* 7.8) 1.2 (+ 5.7)

75.0 ( * 11.3) 85.6 (+ 10.8)

8

2.3 (k9.2)

6.9 ( + 6.4)

5

2.6

9.1 (+ 12.8) 19.8 (+ 7.0)

Gizzard present Bowerbankia gracilis B. imbricata

Gizzard absent Electra pilosa Flustrellidra hkpida

(k3.6)

17.2 (f 5.5)

TABLE IV ANOVA of percentage of ~l~~s~a~~~ valves broken or separated, and broken and separated, in the guts of bryozoans Eowerban~a gracifis, B. Mzicata, Hecpa pifosa, and ~~~e~~dra hispida: NS, not significant. Source of variation Valves broken among groups (species) Gizzard vs. gizzardless B. gracilis vs. F. htkpida E. gracilir vs. E. pirosa 3. bnbricata vs. F. hispida B. imbricata vs. E. pirosa

Error Valves separated among groups (species) Gizzard vs. gizzardless B. B. B. B.

gracik vs. F. htpida gracilis vs. E. pilosa imbricata vs. F. hispida imbricata vs. E. pilosa

d.f

3 1 1 1 1 1 17 3 1 1 1 1

1 Error 17 Sum of valves broken and separated 3 among groups (species) Gizzard vs. gizzardless 1 3. gracik vs. F. hispida 1 8. gracilis vs. E. pi&a 1 3. mascara vs. F. htkpida 1 3. imbrfcata vs. E. pi&a 1 Error 17

ss

31835 31187 11040 12964 16728 20765 1654 1066 680.4 869.4 274.1 640 99.09 661.1 23727 23166 5713 9468 10824 1799.5 2054

MS

10612 31787 11040 12964 16728 20765 97.3 355.3 680.4 869.4 274.1 640 99.09 38.89 7909

23166 5713 9468 10824 17995 120.9

F

109.0 326.6 113.4 133.2 171.9 213.4

9.135 17.49 22.36 7.048 16.46 2.548

65.43 191.7 47.27 78.33 89.55 148.9

P


< 0.001 < 0.05 < 0.05 < 0.05 <0.05 NS


J. B. MARKHAM AND J. S. RYLAND

28

TABLE V Comparison of the percentage of Nirzschia closterium frustules broken or with separated valves after passage through the gut of bryozoans with and without a gizzard: means k SD in parentheses.

Species

Number of replicates

Percentage broken

5

33.6 (+ 13.8)

5 5

13.6 8.4

Percentage separated

Percentage broken or separated

Gizzard present Bowerbankia imbricata

3.0

(k2.1)

36.6 (+ 13.6)

Gizzard absent Electra pilosa Flustrellidra hispida

NITZSCHIA

14.2 ( f 11.8) 30.8 (f 13.2)

(+ 5.4) (k9.0)

27.8 ( f 16.9) 39.6 (+ 14.4)

CLOSTERIUM

Percentages were determined as for Thalassiosirafluviatilis (Table V) and the same statistical methods used. Mean percentage broken in Bowerbankia imbricata was greater than in either Electra pilosa or Flustrellidra hLspida (Table VI: P < 0.05). Mean percentages of separated valves in F. hispida, Electra pilosa and Bowerbankia imbricata

TABLE VI ANOVA of percentages of Nitzschia closterium valves broken or separated (the latter transformed to logarithms) in the guts of bryozoans Bowerbankia imbricata, Electra pilosa and FlustreUidra hispida. Source of variation Valves broken among groups (species) Gizzard vs. gizzardless B. imbricara vs. F. hirpida B. imbricata vs. E. pilosa

Error Valves separated among groups (species) Gizzard vs. gizzardless B. imbricara vs. F. hispida B. imbricata vs. E. pilosa

Error

d.f

ss

2 1 1 1 12

1770 1703 1588 1000 1200

2 1 1 1 12

2.984 2.585 2.918 1.159 1.071

MS

F

P

885.1 1703 99.97 1000 100

8.85 17.0 15.9 10.0

< 0.005 <0.05 < 0.05 < 0.05

16.72 28.96 32.69 12.99


1.492 2.585 2.918 1.159 0.089

decline progressively. These values were transformed to log,, (PVS) to reduce heterogeneity of the variances. The difference between the mean of B. imbricata and that of either Flustrellidra hkpida or Electra pilosa was significant (P < 0.01: Table VI). The greater ability of the two gizzardless species in separating valves was sufficient to negate the advantage that Bowerbankia imbricata had in breaking open frustules, and the sum of percentages broken plus separated is similar for all three species.

FUNCTION OF THE GIZZARD IN BRYOZOANS

29

TABLE VII The number of tentacles per lophophore in gizzard-bearing bryozoans (from Prenant & Bobin, 1956, unless otherwise indicated): Penetrantia and Spathipora sp. are included although the “gizzard” is an unchitinized proventriculus, as is Hislopia in which the chitinized proventriculus has only a storage function; Avenella and Terebrtpora are omitted (see p. 32). Species

Number of tentacles Ctenostomata Vesicularioidea

Vesiculariidae Amathia ahernata A. convoluta A. distans A. lendigera A. pruvoti A. sem~~onvoluta A. vidovtci 3owerba~a &&a 8. gracilis 3. ~a&il~ima 3. imbrikata 3. maxima B. pustulosa Vesicularia spinosa Watersiana paessleri Zoobottyon verticillatum

8 (Winston, 1978) 8 (Harmer, 1915) 8 8 8 Markham (pars. obs.) 8 (Calvet, 1900) 8 8 8 8 10 8 (Winston, 1982) 8 8 9 (Calvet, 1912, as Waters&t) 8

Buskiidae Bushia nitens B. seriata 8. socialis

8 8 (Osburn & Soule, 1953)

8

Spathiporidae Spathipora comma S. mazatlanica S. eltaninae S. varians Spathtpora sp.

8 (Soule, 195Ob, as Terebr@ora) 8 (Soule t Soule, 1976, as Terebrtpora) 10 (Soule & Soule, 1968, as Terebripora) 11 (Soule 8c Soule, 1969a, as Terebripora) 12 (Marcus, 1938, as T. ramosa) Walkerioidea

Aeverrilliidae Aeverrtilia armata A. setigera

8 (Winston, 1978) 8 (Harmer, 1915; Osburn & Soule, 1953) Victorelioidea

Victorellidae Bai~~la abscond~a

8 (Braem, 1951) Hislopioidea

Hislopiidae ~~lopia corderoi H. lacustnk H. placoides H. malayens&

12 (d’Hondt, 1983) 16-18 (d’Hondt, 1983) 8 (d’Hondt, 1983) x 16 (Annandale, 1916)

J.B. MARKHAM AND J. S. RYLAND

30 TABLEVII (continued)

Number of tentacles

Species Incertae sedis Family? Cryptopolyzoon concretum C. evelinae C. wilsoni

14 (Dendy, 1888) 9-10 (-12) (Marcus, 1941, 1942) lo-12 (Dendy, 1888)

Penetrantiidae Penetrantia brevk P. concharum P. densa P. irregularis P. operculata P. parva P. sileni

12 (Siltn, 1946) 10 (Silbn, 1946; Soule, 1950a) 12 (Silk, 1946; Soule, 1950a) 14 (Siltn, 1956) 12 (Soule & Soule, 1969a) 11 (Siltn, 1946) 11 (Soule, 1950a) Cbeilostomata

Hippothoidae Plesiothoa trigemma

10 or 11 (Ryland & Gordon, 1977, as Hippothoa) Cyclostomata

Annectocymidae Annectocyma major A. tubulosa

15

15

(Schafer, 1986a. Annectocyma introduced by Hayward & Ryland, 1985, for Diaperoecia in part)

Frondiporidae Fasciculipora/Frondipora sp.

15-16 (Boardman 8c McKhmey, 1986)

Pustuloporidae Pustulopora sp.

?

TABLE VIII Frequency distributions of tentacle number in general sample of 212 species of marine bryozoans (Winston, 1977), in 40 species of gizzardless stolonate Ctenostomata (from Table VII and d’Hondt, 1983), and in a sample of 30 gizzard-bearing species (from Table VII, excluding Hislopia, Penetrantia. Spathipora sp., and Cyclostomata): species with ranges overlapping two number groups have been scored 0.5 in each. Frequency of occurrence (% )

Tentacle number

General sample

Stolonate gizzardless Ctenostomata

Giizardbearers

8-10 11-13 14-16 17-19 20-22 23-25 26-28 29-31

21.2 25.5 20.8 10.8 9.0 8.0 3.8 0.9

36.3 31.3 15.0 11.3 3.8 2.5 0 0

88.3 8.3 3.3 0 0 0 0 0

FUNCTIONOF THE GIZZARDIN BRYOZOANS

31

TENTACLENUMBER The number of tentacles comprising the lophophore in most known gizzard-bearing bryozoans is given in Table VII. These numbers are expressed as a frequency distribution in Table VIII. The frequency distribution mers from that in both gizzardless stolonate ctenostomes (Kohuogorov-Smimov two-sample test (Sokal & Rohlf, 1981), P < 0.001) and an overall sample of 212 bryozoan species (P -C 0.001). Including the three species of Cyclostomata in column three does not alter these significance levels. DISCUSSION ABILITYTO CRUSH DIATOMFRUSTULES The gizzard-bearing species (except A~thju pruvoti and Bowerbank~a citrina) had a si~i~c~~y greater (P < 0.05) ability to break open the frustules of diatoms than the two gizzardless species. Percentages broken were 2%84% in the ~zz~d-~~~rs and < 14% in the others. ‘Ihe large size of Fi~~e~~ra hisp~dadoes not increase its ability to break frustules. ABILITYTO SEPARATEDIATOMVALVES The mean percentages of Thalassiosira jluviatiks and Nitzschia closterium frustules opened unbroken by gizzardless species (7-17 y0 and 14-3 1%) respectively) are greater (P < 0.05) than in Bowerbunkiu gracilis and B. imbricata (< 3%). The greater ability of Flustrellidra hispida and Electra pilosa to separate the frustules of Nitzschia closterium unbroken (P < 0.01) was sufftcient to negate the advantage of Bowerbankia imbricata in breaking them open, the percentage opened plus broken being similar in all three bryozoans (28-40%). Species lacking a gizzard have, therefore, some ability to exploit the diatom resource. SELECTIVEADVANTAGESCONFERREDBY A GIZZARD Armoured exoskeletons are present in several groups of plankton: (1) diatoms, with those that live inshore having a more strongly silicified wall than non-neritic species (Lebour, 1930); (2) thecate dinoflagellates, with a theta of two to many interlocking cellulose plates; (3) si~cofl~ellates, with a skeleton of ~terconnect~g siliceous rods forming radiating spines; (4) radiolarians, in which the skeleton is mainly silica {see Schafer, 1986b, for discussion of occurrence); and (S)cocco~thophores, with calcareous coccoliths. The last may be important in tropical areas, less so in neritic temperate waters. Different major groups within the phytoplankton have greatly different ranges in cell volume (Harvey, 1950). If these volumes are expressed in terms of the diameter of a sphere of equal volume, the ranges are: diatoms 3-340 pm, dinoflagellates lo-58 pm, microflagellates and coccolithophores 3-10 pm.

32

J. B. MARKHAM AND J. S. RYLAND

Diatoms are usually the most conspicuous members of the British coastal phytoplankton with respect to size and numbers, with dinoflagellates second. The classical seasonal cycle is characterized by a spring outburst of conspicuous diatoms, followed by a summer peak of dinoflagellates (Smayda, 1980). This is the pattern in the vicinity of Swansea (Sexton, 1984). In the net plankton it is difficult to fmd diatoms sufficiently small to be ingested by gizzard-bearing bryozoans. 3. grucilis, for example, ingests T~a~assiosiru~via~~ with difliculty. While some small diatoms are spiny and/or form chains which cannot be ingested, it has in recent years been demonstrated that very small diatoms (diameter < l-2 ,um) may comprise a sign&ant part of the nanoplankton (Raymont, 1980), both in the tropics (Collier & Murphy, 1962) and in temperate waters (Sexton, 1984). There is still a shortage of ~fo~ation on the t~onomic composition of the nanoplankton. The ability of bryozoans to capture particles depends essentially on the form of the lophophore. Lophophore size is positively correlated with the number of tentacles comprising it (Ryland, 1975; Winston, 1977). Completing an accurate survey of tentacle number in gizzard bearers has proved unexpectedly dficult. Surprisingly, this was less on account of the absence of records of tentacle number than on the meagre desc~ptions of the structure of gizzard-like organs in the gut in many of the species. Table VII includes two genera (~~~~~~a~Wat~rsia~a~overlooked in the tabulations of Gordon (1975a), Ryland (19761, and Schtier (1986b), and deletes the spurious Avenella (see Hayward, 1985). Its compilation led to a thorough re-examination of the literature on P~~~antia, Tereb~~ra, and ~pat~~ra, three genera usually found in old mollusc shells and characterized by their ability to dissolve calcified structures. The species of Penetrantia do not have a true gizzard but “a rounded cardia.. . often inconspicuous.. . between 20 and 25 microns in diameter [which] opens into the stomach pouch [caecum]. Histological sections show its wall to be composed of the longitudinal and obliquely arranged layers of muscle [cf. the circular band in Vesiculariidae], with the lumen lined by a low simple columnar epithets that is devoid of keratinization” (Soule & Soule, 1975). Moreover, in contrast to the true gizzardbearers, the pylorus does produce a rotating cord (Siren, 1947). Soule & Soule (1969a, 1975) argue that Penetrantiu should properly be classified with the Cheilostomata, but this view is strongly refuted by Pohowsky (1978). The status of Tereb~ra is confused. The type is T. ramosa, a nominal species re-described by Marcus (1938). However “although some of the specimens figured by Marcus [as T. ramosa] belong to Terebripora, the colony or colonies whose sofi parts he examined certainly do not. Subsequent assignments of species to Terebripora on the basis of internal features comparable to those described by Marcus are of tenuous validity” (Pohowsky, 1978). “T. ” comma, “T. ” e~tan~naeand “T. ” varzims, following Pohowsky, are here treated as species of ~p~t~i~ra. If Pohowsky’s further su~estion that an illustration of rrn~~en~ap~~~pi~~~ (Soule, 1950a, Pl. 1, Fig. 5 [not Fig. 1G as Pohowsky states]) “is certainly representative of Terebriyora”, then Terebripora also lacks a gizzard.

FUNCTION OF THE GIZZARD IN BRYOZOANS

33

Sputhiporu emerges from this analysis as a catch-all, and Pohowsky was surely in

error to denigrate the taxonomic value of internal anatomy. The type, S. serum, is at present unrecognizable (Pohowsky, 1978) and its soft parts undescribed. The gizzard of S. comma was noted by Soule (1950b) only as “prominent globular” but Bobin & Prenant (1954) subsequently provided a full, illustrated account, and one must agree with their diagnosis that the gizzard is characteristically vesicularioid, with teeth of two sizes and an equatorial muscle band. S. mazutlunicu (Soule & Soule, 1976) has “a digestive tract of which the most distinctive feature is a prominent gizzard with chitinized denticles” (authors seem to have used “chitinized” and “keratinized” interchangeably but the latter must be presumed incorrect). Both S. eltuninue (Soule & Soule, 1968) and S. vuriuns (Soule & Soule, 1969b) have a “prominent grinding organ or gizzard” although neither text nor illustrations provide amplification. Sputhiporu sp. (Marcus, 1938, Fig. 2D), erroneously included within the account of Terebriporu rumosu (fide Pohowsky, 1978), does not have a gizzard at all, but a globose and muscular, unchitinized proventriculus, corresponding to that of Victorella (Marcus, 1938). It is obviously not congeneric with the other species mentioned. The frequency distribution of tentacle number in gizzard-bearing species was significantly lower than that in a random sample of all Bryozoa (P < 0.001). The former usually have only 8-10 tentacles, except in the cyclostome genera, whereas other bryozoans frequently have up to 25 tentacles and sometimes more (Table VIII). Perhaps even more interesting is the comparison between gizzard-bearing and gizzardless stolonate ctenostomes. The frequency distributions are again significantly different (P < 0.00 1). Cyclostome lophophores do not emerge fully from their zooids and a strict comparison between Cyclostomata and Cheilo-Ctenostomata is perhaps not valid. Accordingly, the cyclostomes were omitted from Table VIII but it should be noted that their inclusion does not significantly change the probability levels (P < 0.001) for the group comparisons. Tentacle number and mouth diameter are positively correlated (Winston, 1977). Thus, many gizzard bearers have a mean mouth diameter of %20-30 pm (Winston, 1978) close to the minimum size of many diatoms. Nominal mouth diameter is, however, an unreliable estimate of the maximum size of particle that can be ingested. Buccal dilatation can increase mouth diameter in Cryptosulupufkzsiunu (17 tentacles) by ~30% (Gordon, 1974); and in Flustrellidru hispidu (27-30 tentacles), which has a relaxed mouth diameter of 44 pm (Dyrynda., pers. comm.) or a nominal diameter of 90 pm (Winston, 1977), dilatation must be able to extend the mouth by = 140x, because a solid sphere 105 pm diameter has been observed in faeces (Markham, pers. obs.). In Bowerbunkiu imbricuta (only 10 tentacles, nominal mouth diameter 33 or 22 pm (Winston, 1977, 1978, respectively)) buccal dilatation can exceed 90% because pollen grains 42 pm in diameter are readily ingested (Markham, pers. obs.). (Unfortunately, a comparison of the features of the nominal species B. imbricutu and B. grucilis in Ryland (1975: New Zealand), Winston (1978: North and Central America) and Hayward (1985 : British Isles) suggests that more than two species are involved. Indeed, Winston (1982) later described another species, B. maxima.)

34

J. B. MARKHAM AND J. S. RYLAND

Bryozoans with eight tentacles have a relaxed mouth diameter of z 15-25 pm (Winston, 1978). If this can be increased by up to 100x, then such a species could ingest particles of up to only 30-50 pm diameter. Thus, the small lophophore of a majority of gizzard-bearers seems to exclude them from effectively exploiting a large portion of the available diatom resource. If exploiting the diatom resource were the primary selective advantage derived from a gizzard, it is paradoxical that this advantage should not accrue to species with large lophophores. There is no apparent evidence that gizzard-bearers are restricted to habitats particularly rich in the smallest diatoms. Although a gizzard is not present in all small bryozoans (e.g., Walkeria uva, eight tentacles; crisiids, eight or nine tentacles; aeteids, x 12 tentacles), a gizzard may confer one or more of the following benefits. (1) Expansion of the particle size continuum which is utilizable. Small species have a proportionally narrow intestine, requiring that food particles be small. As the mouth can open much wider than the diameter of the intestine, the gizzard would then reduce ingested particles to a size capable of passing into the intestine. For example, Bowerbankia imbricata (10 tentacles) can actually ingest somewhat larger particles than Cryptosulapallasiana (17 tentacles); and of Walkeria uva and Bowerbankia gracilis (each with eight tentacles) only the latter can ingest Thafassiosira jluviatilis (Markham, pers. obs.). (2) While all bryozoan guts have thin walls (Gordon, 1975c), narrow guts probably produce weaker contractions. This may reduce the ability to rupture cell walls. Electra pilosa in culture grows well on the haptophycean Chrysochromulinapolylepis mainly, it appears, because its digestive enzymes more effectively destroy cell walls of that species than those of Isochrysis or Dicrateria (Jebram, 1982a). Any difficulty that small bryozoans have in digesting cell contents through intact cell walls would be eliminated by the presence of a gizzard. (3) Perhaps gizzards are restricted to small species for an indirect reason. Suspended fine material precipitates in estuaries and many gizzard-bearers seem adapted to estuarine or silt-laden habitats (e.g. Bowerbankia spp.). The stolonate habit, often developed into epibiosis or free tufts, characterizes nearly all gizzard-bearers and may be adaptive in reducing the adverse effects of siltation (see Jackson, 1979). It is commonest in species with small lophophores because they are energetically efficient (Ryland & Warner, 1986; Markham, in prep.). A gizzard may allow estuarine bryozoans to exploit small dinoflagellates, which are sometimes abundant in estuaries (Perkins, 1974; Raymont, 1980) especially in summer, and seston. Marine bacteria tend to adhere to, and concentrate on, the surface of suspended dead organic material (Oppenheimer & Vance, 1960). Small diatoms are associated with the sediment, and are made available by turbulence, but large planktonic diatoms generally predominate in spring. The rotating cord (ergatula) in the pylorus is one of the characteristic features of the gut of Gymnolaemata and Stenolaemata (Silen, 1944). It is not clear from SilCn’s paper which gizzard-bearing species are known to lack the rotating ergatula, and it would be particularly interesting to know whether this applies to non-vesicularioid gizzardbearing bryozoans (we have already noted its presence in Penetrantia). Siltn regarded the ergatula as facilitating digestion (as in bivalves and some gastropods); Gordon

FUNCTION OF THE GIZZARD IN BRYOZOANS

35

( 1975~) considered compaction of particles, prior to the formation of a faecal pellet, to be the main function. It is not immediately apparent how the presence of a gizzard would afTect the latter role, whereas comminution of cells is an obvious step towards their digestion. Despite the demonstration in this paper of unambiguous benefits, no further light seems shed on the question why the gizzard is found only in bryozoan species with small zooids: that enigma remains unresolved.

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SILBN,L., 1944.On the division and movements ofthe alimentary canal ofthe