And Bulinus Tropicus (Indigenous) in Relation to Recolonisation

Observations on the radulae of Physa acuta (invasive) and Bulinus tropicus (indigenous) in relation to recolonisation

Observaciones sobre las rádulas de Physa acuta (especie invasora) y Bulinus tropicus (indígena) en relación con la recolonización

Therese D. BRACKENBURY*

Recibido el 16-II-1999. Aceptado el 22-VII-1999

ABSTRACT In South Africa the invasive snail, Physa acuta, has repeatedly shown its ability to rapidly recolonise denuded habitats after flooding of the Umsindusi River. This was not the case for indigenous species, such as Bulinus tropicus, which were dependent on the return of marginal vegetation. Although previous investigations revealed that P. acuta possessed several attributes which contribute to its success, its feeding strategy in a denuded habitat was unknown. The present investigation found that the radula of P. acuta appeared to be adapted for harvesting/combing fine detritus or unicellular organisms (0.5 to 10 µm) while that of B. tropicus was adapted for rasping large sized food particles and filamentous algae (≥ 20 µm). The denuded substratum of the Umsindusi River was noted to be abundant in unicellular organisms while filamentous algae and detritus remained absent until the return of marginal vegetation. Therefore, it is possible that the radular structure and feeding mechanism of P. acuta was another contributing factor to its success as a colo- niser.

RESUMEN El caracol invasor Physa acuta ha mostrado repetidamente su capacidad para recolonizar hábitats arrasados por avenidas del rio Umsindusi en Sudáfrica. Por el contrario, algunas especies autóctonas, como Bulinus tropicus, necesitaron una previa revegetación de las áreas devastadas. Aunque investigaciones precedentes señalaron que P. acuta posee varias características que favorecen este éxito en la recolonización, se desconce como influye en ella su estrategia trófica. Esta investigación pone de manifiesto que la rádula de P. acuta parece estar adaptada para ramonear sobre detritos finos y organismos unicelu- lares (0,5 a 10 µm), mientras que la de B. tropicus está adaptada a hacerlo sobre particu- las alimenticias mayores y algas filamentosas (≥ 20 µm). Se halló que los organismos uni- celulares pequeños son abundantes en el sustrato desnudo del rio Umsindusi, mientras que éste carece de algas filamentosas y de partículas grandes hasta que se repuebla con vegetación. Por ello, la estructura de la rádula y la estrategia trófica de P. acuta se consi- deran factores que contribuyen a su éxito como colonizador.

KEY WORDS: radula, feeding mechanism, invasive, Physa, Bulinus. PALABRAS CLAVE: rádula, estrategia trófica, invasiones, Physa, Bulinus.

* Biological Control Products Pty (Ltd), PO Box 1561, Pinetown 3600, South Africa.

85 Iberus, 17 (2), 1999

INTRODUCTION

The invasion by aquatic pulmonates in the river; these included year-round has been increasing in the rivers of sout- breeding, high intrinsic rate of increase, hern Africa and a species of particular broad thermal and high water current interest in South Africa is the North velocity tolerance, the absence of patent American aquatic snail, Physa acuta (Pul- trematode infection (BRACKENBURY AND monata: Physidae) (Draparnaud 1805) APPLETON, 1993, BROWN, 1994) and (BROWN, 1980). It has become establis- negligible predation (WILKENAND hed in many of South Africaís river APPLETON, 1991). Bulinus tropicus on the systems (HAMILTON-ATTWELL, DE KOCK other hand did not possess these traits AND VAN EEDEN, 1970; DE KOCK, (BRACKENBURY, 1989; BRACKENBURY AND JOUBERT AND PRETORIUS, 1989). The snail APPLETON 1991, 1993). has been recorded sporadically in the In a denuded river habitat, such as Umsindusi River (KwaZulu-Natal Pro- the Umsindusi River, snails attempting vince), but since 1986 the species has to recolonise an area would encounter, comprised between 66 - 94% of the local amongst others, difficulties in locating a gastropod population (BRACKENBURY readily available food supply. BRACKEN- AND APPLETON, 1993). In 1987-88 the BURY (1989) noted that newly establis- Umsindusi River was flooded on four hed P. acuta populations fed off a rich occassions which extensively eroded the diatom resource on the Umsindusi river channel removing all marginal channelís substratum. Although this vegetation and the associated fauna. food supply was available in regions of However, P. acuta rapidly (30-90 days) low water current velocities, B. tropicus, recolonised the denuded bed on each only recolonised the area after marginal occasion and in due time comprised vegetation had returned. Plants not only between 80 - 100% of the gastropods provide protected holdfasts for the present. The most common indigenous snails, but also an alternative food species, Bulinus tropicus, however, never resource such as epiphytic algae, deca- exceeded 20% (BRACKENBURY, 1989). ying macrophytes and fine detrius Physa acuta was observed to possessed (PIMENTAL AND WHITE, 1959; CALOW, an number of attributes which appeared 1970; HUNTER, 1980; THOMAS, 1987; to contribute to its success as an invader MADSEN, 1992). The question then arose:

(Right page) Figure 1. Physa acuta SEM. A: triangular jaw composed of a thin dorsal plate overlying numerous pillar-like structures; B: radular ribbon fully displayed showing symmetrical arrangement of teeth; C: nascent region with newly formed central teeth (single row) and lateral teeth (multiple rows on either side of central row); D: mid-region of ribbon supporting mature teeth; E: anterior region of ribbon which supports the old and worn teeth. Scale bars, A, C, E: 20 µm; B: 600 µm; D: 50 µm. Abbreviations, a: anterior end; al: algae; c: central teeth; cr: central longitudinal row of teeth; e: cutting edges of jaw; l: lateral teeth; p: dorsal plate; pi: pillar-like structures; po: posterior end; r: region cleared of algae by the radula. (Página derecha) Figura 1. Physa acuta MEB. A: mandíbula triangular compuesta por una fina placa dorsal que recubre numerosas estructuras en forma de pilar; B: rádula completa mostrando la disposición simétrica de los dientes; C: región de crecimiento con dientes centrales recien formados (una única línea) y dientes laterales (varias líneas a cada lado de la central); D: región media de la rádula, con dientes maduros; E: región anterior de la rádula con dientes viejos y deteriorados. Escalas, A, C, E: 20 µm; B: 600 µm; D: 50 µm. Abreviaturas, a: borde anterior; al: algas; c: diente central; cr: fila central de dientes; e: borde cortante de la mandíbula; l: dientes laterales; p: placa dorsal; pi: estructuras en forma de pilar; po: borde posterior; r: áreas libres de algas por efecto de la rádula.

86 BRACKENBURY: Radulae of Physa acuta and Bulinus tropicus in relation to recolonisation

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87 Iberus, 17 (2), 1999

does the radula structure and rasping tered onto micropore filter paper (pore mechanism play an important role in size 0.45 µm) coated paper was submer- contributing to the ability of P. acuta and sed in water over which individual B. tropicus to invade and colonise a snails (n= 10) (starved for two days) barren habitat? The present study were allowed pass over. The papers attempted to answer this question. were then removed, fixed in 3% glute- raldehyde in 0.05M phosphate buffer, MATERIAL AND METHODS critical point dried, carbon coated and viewed under a dissecting microscope Adult P. acuta and B. tropicus, with and SEM. To observed the ability of the shell heights of 6.0 - 6.5 mm and 7.0 - 7.5 radula of each species to collect different mm (median shell height) respectively, sized food particles, microspheres (0.5 were collected from a pond in, Durban, µm), unicellular algae such as Selenas- South Africa (29° 49’ S; 31° 01’ E) and ac- trum capricorn (6-7 µm), Bumilloeriopsis climatized in pond water in the labora- sp. (10-12 µm), and the filamentous alga tory for seven days. To study the struc- (18-20 µm) were collected separately on ture of the radula ribbon, the buccal micropore filter paper as described mass (n= 8) of both P. acuta and B. tropi- above. Individual snails (n= 10) were cus were removed from freshly killed allow to move and feed once over the snails and placed in a 5 ml solution of paper which was then prepared as des- potassium hydroxide (± two pellets) and cribed above. Average particle densities heated in a water bath (70°C) for two to before and after feeding were calculated five minutes. After the dissolution of the from SEM micrographs. tissue the radular ribbon and attached jaw were isolated in 70% ethanol, soni- cated and then mounted flat in a drop of RESULTS ethanol on double sided tape. This was followed by gold-palladium coating Morphology: The roof of the buccal (Poleron E5100 SEM Coating Unit) and cavity of P. acuta (shell heights between viewed with a Hitachi F520 Scanning 6.0 and 6.5 mm) supported a single, thin Electron Microscope (SEM). Live move- light brown, transverse triangular jaw ment of the radula and odontophore (171 µm x 37 µm). SEM examination was recorded using a VRC as snails (n= showed that the jaw was composed of a 10) travelled over algal coated Petri-dis- thin dorsal plate overlying numerous hes. To obtain the feeding track pattern flat-ended pillar-like structures (Figure of the two species the green unicelluar 1A). The odontophore supported a ra- alga, Chlamydomonas sp. (10 µm) was fil- dular ribbon, a highly malleable mem-

(Right page) Figure 2. Bulinus tropicus SEM. A: the thick, darkly pigmented, sickle-shaped jaw with a narrow cutting edge; B: radular ribbon fully displayed showing symmetrical arrangement of teeth; C: nascent region with newly formed central teeth (single row) and lateral teeth (several rows either side of central row); D: newly formed and maturing marginal teeth which are located on the marginal edges of the ribbon; E: anterior region of the ribbon supporting extensively worn central and lateral teeth. Scale bars, A: 100 µm; B: 350 µm; C, D: 20 µm; E: 30 µm. Abbreviations as in Figure 1. (Página derecha) Figura 2. Bulinus tropicus MEB. A: mandíbula gruesa, oscura, en forma de hoz, con un borde cortante estrecho; B: rádula completa mostrando la disposición simétrica de los dientes; C: región de crecimiento, con dientes centrales recien formados (una única línea) y dientes laterales (varias líneas a cada lado de la central); D: dientes marginales recien formados, localizados en los bordes de la rádula; E: región anterior de la rádula, con dientes muy gastados. Escalas, A: 100 µm; B: 350 µm; C, D: 20 µm; E: 30 µm. Abreviaturas como en la Figura 1.

88 BRACKENBURY: Radulae of Physa acuta and Bulinus tropicus in relation to recolonisation

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89 Iberus, 17 (2), 1999

brane to which numerous symmetrically narrow cutting edge (Figure 2A) and the arranged teeth were attached. The rib- radular ribbon (averaging 1684 µm long bon of P. acuta (shell height 6.7 mm - 7.5 and 670 µm wide) supported three mm), averaged 1733 µm long and 567 morphologically distinct groups of teeth µm wide (Figure 1B), and covered an with an average density of 5882 area of 5.3 mm2 supporting approxima- teeth/mm2 (Figure 2B, C, D). The teeth tely 5 x 104 teeth (9434 teeth/mm2). morphologies observed in this study Longitudinal rows of teeth were identi- were similar to that described by STI- cal only varying in size depending on GLINGH ETAL., (1962), however, the maturity. The ribbon was symmetrically variation in shape of the central cusps divided by the longitudinal row of cen- was considered to be a consequence of trals flanked on either side by up to 40 wear and tear by the present author. In oblique rows of laterals. Morphologi- comparison to P. acuta, the teeth on the cally distinct marginals were not evi- radula of B. tropicus were fewer in dent. The centrals and marginals appea- number, but larger in size and robust- red delicate which implied that they ness, however, the extent of cusp wear were not used for cutting bulk foods. was far greater in B. tropicus. In the mid- The small centrals were composed of a region of the ribbon the cusps had lost rectangular base (9.9 x 6.76 µm) from 78% of their length and nearly 100% at which projected five cone-shaped cusps the anterior region (Figure 2E). (length 1 to 3 µm) (Figure 1C). With the larger laterals the laterobasal and basal Functional behaviour: The mouth of edges of the pyramidal stem were con- P. acuta was encircled by two lobes of a cave (Figure 1C). The apex of the stem single lip which lead into the buccal ca- expanded into the crown (width 12.76 vity by a short oral tube. When at rest µm) which had five large cusps (average the lateral lobes were apposed longitu- length 5.83 µm) and six small intertitial dinally along the longitudinal axis sea- cusps (average length 2.2 µm). The nas- ling the mouth closed with the jaw fully cent region of the ribbon supported the retracted. The resting odontophore was newly formed teeth which were prolap- folded along its longitudinal axis into a sed and soft with finely point cusps tight U-shaped groove with edges of the while with each consecutive transverse lateral pillars curled under. The radular row the teeth increased in size, and be- ribbon covered most of the cartilage la- came more erect. Sequential rows of te- ying in itís concavity and convex surfa- eth showed slight, progressive and even ces. At the onset of the rasping cycle the wearing of the cusps (Figure 1D, E). lateral lobes of the lip moved away from Those of the centrals were reduced by each other forming a circular opening to 17% while the cusps and intertitial the mouth. The jaw was exposed while cusps of the laterals were reduced by the odontophore cartilage was rotated 43% and 24.5% respectively (Figure 1E). forwards and downwards in the buccal A description of the jaw and radula mass and protracted through the mouth B. tropicus has been provided by STI- towards the substratum. The horizontal GLINGH, VAN EEDENAND RYKE (1962) edge of the “U” (the central region of and STIGLINGH AND VAN EEDEN (1976) the odontophore), also referred to as the and will not be expanded in this text. In “tip”, made the initial contact with the the present study the jaw of B. tropicus substratum and as the odontophore con- (shell height between 7.0 and 7.5 mm) tinued its rotation the pillars of the “U” was similar to that observed by STI- were extended outwards and down- GLINGH, VAN EEDENAND RYKE (1962) wards forming a semi-circular fan-sha- and STIGLINGH AND VAN EEDEN (1976), ped disc (Figure 3A). At the same time however, lateral jaws were not noted. the radular ribbon moved over the ad- Unlike P. acuta the jaw of B. tropicus was vancing edge of the cartilage. In this in- a dark pigmented, well developed, verted position the anterior surface of sickle-shaped dorsal plate with a the radular teeth faced the central row

90 BRACKENBURY: Radulae of Physa acuta and Bulinus tropicus in relation to recolonisation

al r cr

A C

B Figure 3. Physa acuta SEM. A: radula in situ resting on the ”U” shaped odontophore with the wings extended; the row of central teeth forms the ”dividing line” of the ribbon; B: schematic diagram of radula movement during a rasping stroke; the ”E”s represent teeth with projecting cusps; the broken dividing line demarcates the position of the central teeth; C: the resultant radular tracer pattern left behind by the wings of odontophore/ribbon complex; the magnification of the trace clearly shows the efficiency of the radula at removing algae from the substratum. Scale bars, A: 10 µm, C: 0.5 µm. Abbreviations as in Figure 1. Figura 3. Physa acuta MEB. A: rádula in situ, sobre el odontóforo en forma de ”U” con las alas exten- didas; la fila de dientes centrales hace de línea media de la rádula; B: esquema del movimiento radular durante la maniobra de raspado; las “E”s representan dientes con sus cúspides; la linea quebrada indica la posición de los dientes centrales; C: patrón de marcas dejado por las alas del complejo rádula/odontó- foro; la ampliación muestra claramente la eficiencia de la rádula para levantar las algas del sustrato. Scale bars, A: 10 µm, C: 0.5 µm. Abreviaturas como en la Figura 1.

of teeth. The pillars of the cartilage were substratum and rotated back into the then drawn together resulting in the an- mouth. The jaw was not thought to play terior face of the marginals being direc- a significant role in the feeding cycle. ted through the algae (Figure 3B). To- Unlike P. acuta, the lip lobes of B. tro- wards the end of the rasping stroke the picus were prominent, separating asym- odontophore was lifted up from the metrically with the emergence of the

91 Iberus, 17 (2), 1999

Figure 4. Bulinus tropicus SEM. A: radula in situ resting on the odontophore; B: radular tracer pattern showing the incomplete removal of unicellular algae from the substratum. Scale bars, A: 100 µm; B: 260 µm. Figura 4. Bulinus tropicus MEB. A: rádula in situ colocada sobre el odontóforo; B: marcas que deja la rádula, mostrando una eliminación incompleta de las algas del sustrato. Escalas, A: 100 µm; B: 260 µm.

wide, scoop-shaped odontophore follo- and will therefore not be repeated in this wed by the projection of the jaw (Figure paper (Figure 4C). In B. tropicus the bur- 4A). The application of the odontophore den of the rasping action was borne by and radula of B. tropicus has been decri- the centrals and inner marginals. bed in detail by STIGLINGH AND VAN The efficiency of the radulae to EEDEN (1970). Compared to P. acuta, the collect different sized food particles radula of B. tropicus appeared fixed to the varied markedly between the two odontophore such that the long rasping species (Table I). Physa acuta was able action was directed forwards and control to amass all particles sizes ranging from soley by the odontophore and worked 0.5 µm (Figure 5) to 12 µm, but the against the jawís cutting edge. radula was less efficient when dealing with the filamentous algae. On the other Feeding observations: The feeding hand the radula of B. tropicus was trail patterns of P. acuta and B. tropicus unable to harvest the microspheres and varied from occasional, isolated rasps to was inefficient at collecting small unice- a continuum zig-zag. The individual llular algae (Table I) as observed by STI- rasps of P. acuta involved the use of the GLINGH AND VAN EEDEN (1970); it only whole radula and consisted of two semi- appeared to be effective when rasping circles hinge posteriorly denoting the filamentous algae in this study. “tip” of odontophore and the position of the central teeth which do not appear to be functionally important in gathering DISCUSSION food (Figure 3C). The radula was effective at removing most of the algae from Freshwater rivers in Africa are the substrate. The rasp patterns of B. tro- dynamic systems that can be dramati- picus were similar to those already decri- cally altered by floods and/or droughts. bed by STIGLINGH AND VAN EEDEN (1970) This severely impacts on the aquatic

92 BRACKENBURY: Radulae of Physa acuta and Bulinus tropicus in relation to recolonisation

Table I. Average densities of microspheres and algae before and after the feeding action of Physa acuta and Bulinus tropicus. Tabla I. Densidades medias de microesferas y algas antes y depues de la depredación de Physa acuta y Bulinus tropicus.

Physa acuta Bulinus tropicus Efficiency Efficiency Organism Density before Density after Density before Density after of removal (%) of removal (%)

Microspore (0.5 µm) 750/500 µm2 17/500 µm2 97.7 750/500 µm2 739/500 µm2 1.5 Selenastrum capricorn (6-7 µm) 360/500 µm2 2/500 µm2 99.4 360/500 µm2 301/500 µm2 16.3 Bumilloeriopsis sp. (10-12 µm) 340/500 µm2 25/500 µm2 92.6 340/500 µm2 199/500 µm2 58.5 Scenedesmus sp. (18-20 µm) 143/500 µm2 71/500 µm2 49.6 143/500 µm2 9/500 µm2 93.7

vegetation and the associated fauna. In NET, 1995). A few species have been 1987 and 1988 the Umsindusi River found to be selective for filamentous system was profoundly disturbed by algae e. g. Lymnaea peregra, or diatoms e. flooding on four separate occasions. The g. Planorbis vortex (LODGE, 1986), but invasive snail, P. acuta, was able to re- overall pulmonates are non-selective establish itself in significant numbers omnivors and the food dimensions are within one to three months in the only restricted by the structure of the absence of aquatic vegetation (BRACKEN- radula (STIGLINGH AND VAN EEDEN, BURY, 1989). This was possibly due, in 1970; HUNTER, 1980; MADSEN, 1992). part, to a number of characteristics pos- BRACKENBURY (1989) observed that P. sessed by P. acuta viz. high intrinsic rate acuta utilised the rich supply of diatoms of natural increase and water current in the denuded habitat of the Umsin- velocity tolerance, year-round breeding, dusi River, however, B. tropicus, remai- and the lack of predation and parasi- ned absent even from quiescent pools of tism. Bulinus tropicus reappeared at a the river regardless of the fact that low density nine months or more after diatoms were a supposed favoured food the initial flooding. This coincided with (STIGLINGH AND VAN EEDEN, 1970). the return of aquatic vegetation. A The rasping action of P. acuta can be similar pattern was found with Bulinus described as a combing or mopping mo- truncatus in Morrocco (KHALLAAYOUNE, vement (STIGLINGH AND VAN EEDEN, LAAMRANI AND MADSEN, 1998; KHALLA- 1970) with the radula and odontophore AYOUNE, MADSEN AND LAAMRANI, 1998). work concurrently, but independently of The study by BRACKENBURY (1989) sug- each other. SMITH (1988) has called this gested that aquatic vegetation played a mechanism the “moving-conveyor belt- significant role in the growth of Auf- rasp”. At the beginning of the rasping wuchs as well as providing a source of stroke the odontophore cartilage carries decaying vegetation. The diet of P. acuta the radula towards the substrate and de- and B. tropicus in the Umsindusi prior to forms to increase the exposed surface the floods is unknown, but many area of the radula. At the same time the studies have shown that freshwater pul- radular ribbon moves over the cartilage. monates such as lymnaeids, physids During the rasping action the radula and and planorbids feed on epiphytic and odontophore gradually return to their filamentous algae, diatoms, blue-green original positions. As a consequence of algae, detritus and decaying vegetation this movement consecutive rows of teeth (e. g. STIGLINGH AND VAN EEDEN, 1970; are continually rasped through areas RUNHAM, 1975; MADSEN, 1992; ESTEBE- missed by preceeding rows during a sin-

93 Iberus, 17 (2), 1999

Figure 5. Physa acuta SEM, high magnification of the lateral teeth (similar to those in Figure 1E) showing the accumulation of the microspheres (mi) (diameter 0.5 µm) on the underside of the crown and cusps as a result of the radula combing the surface of the substratum. Scale bar 2 µm. Figura 5. Physa acuta MEB, ampliación de un diente lateral (similar a los de la Figura 1E) mostrando la acumulación de microesferas (mi) (diámetro 0.5 µm) debajo de la corona y las cúspides, como conse- cuencia de la curvatura de la rádula sobre el sustrato. Escala 2 µm.

gle feeding cycle. The slight wearing of substratum. With the use of only one the cusps supported the supposition that row of teeth any additional food mate- the teeth of P. acuta lightly comb or mop rial remaining on the substratum would the substratum. This feeding strategy not be collected. The efficiency is further plus the high density of teeth, would ac- reduced by the lower density of teeth count for the efficiency of collecting uni- per unit area in B. tropicus. Therefore, celluar organisms or fine detritus (0.5 the odontophoral lick is considered a µm to 10 µm). Subsequently, P. acuta was relatively inefficient mechanism (SMITH, capable of effectively exploiting the dia- 1988) resulting in the incomplete toms and detritus on the substratum of removal of small algae (STIGLINGHAND the Umsindusi River, thereby contribu- VAN EEDEN, 1970). The radula of B. tropi- ting to the species ability to establish it- cus considered more apt for dealing self in a denuded habitat. with filamentous algae and bulk foods The radula and odontophore of B. as it possesses sharp, robust, cutting tropicus on the other hand had a diffe- laterals (STIGLINGH AND VAN EEDEN rent functional relationship which 1970) and a jaw which works against the SMITH (1988) described as the ìodonto - radula resulting in a additional cutting phoral lickî. In this instance the radula is action. Large unicellular organisms fixed to the odontophore, and thereby would be gathered mostly by the margi- its rasping action is directed and contro- nals. Consequently, B. tropicus was con- lled by the underlying cartilage which sidered to have been ill-equipped to moves post-anteriorly through the subs- harvest the available food resources in tratum. Consequently, only a single the denuded Umsindusi River habitat transverse row of teeth at the edge of and hence its dependent association the odonotphore rasps the substratum with marginal and aquatic vegetation. for the length of the odontophoral The present study showed that the stroke. The severe wearing of the cusps radula structure and feeding mecha- is indicative that the radula is applied to nism of the invasive species, P. acuta the substratum with considerable force was markedly different from those of to break the algae’s attachment to the the indigenous species, B. tropicus. The

94 BRACKENBURY: Radulae of Physa acuta and Bulinus tropicus in relation to recolonisation

radular structure of each species appea- ACKNOWLEDGEMENTS red to determine the range of food resources that they could utilize, which The author wishes to acknowledge in turn partially impacted on their the assistance of Dr Fiona Graham and ability to recolonize the denuded habitat Prof. C. C. Appleton, University of of the Umsindusi River. Natal, Durban.

BIBLIOGRAPHY

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