Macro-invertebrate predators of freshwater pulmonate snails in Africa

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African Journal of Aquatic Science 2004, 29(2): 185–193 Printed in South Africa — All rights reserved

AFRICAN JOURNAL OF AQUATIC SCIENCE ISSN 1608–5914

Macro-invertebrate predators of freshwater pulmonate snails in Africa, with particular reference to Appasus grassei (Heteroptera) and Procambarus clarkii (Decapoda) CC Appleton1*, BV Hofkin2 and A Baijnath1,3 George Campbell Building, School of Life & Environmental Sciences, University of KwaZulu-Natal, Durban 4041, South Africa 2 Department of Biology, University of New Mexico, Albuquerque, NM 87131, United States of America 3 Present address: Forestry and Forest Products Research Centre, University of KwaZulu-Natal, Durban 4041, South Africa * Corresponding author, e-mail: [email protected]

1

Received 10 December 2003, accepted in revised form 7 May 2004

A range of African and alien macro-invertebrates has been reported preying on freshwater pulmonate snails, including those that serve as intermediate hosts for bloodflukes of the genus Schistosoma. Predation by five molluscivorous taxa is reviewed here: indigenous leeches (Glossiphoniidae), marsh fly larvae (Sciomyzidae), waterbugs (Belostomatidae), crabs (Potamonautidae) and invasive crayfish (Astacidae). Common features are a lack of prey specificity but clear prey-size specificity. Attention is drawn to the ability of invasive snail species (Physidae and Lymnaeidae) to avoid predation by several of these taxa. Evidence suggests that only the alien invasive crayfish Procambarus clarkii has potential as a snail biocontrol agent, but that its use should not be encouraged. Keywords: Africa, Appasus, Helobdella, Physidae, Potamonautes, predation, Procambarus, Sepedon

Introduction Freshwater pulmonate snails, including the intermediate hosts of human schistosomes, are preyed upon by a wide variety of invertebrate predators but only five, all macroinvertebrates, have been studied in any detail in Africa. Even fewer have been assessed as snail biocontrol agents for integrated schistosomiasis control programmes. Those that have been studied include indigenous predators (leeches, sciomyzid fly larvae, waterbugs and crabs) and an introduced predator, the crayfish Procambarus clarkii. This contribution reviews what is known of malacophagy by these predators in Africa, but concentrates on recent studies on predaceous waterbugs and the invasive P. clarkii. In doing so, we draw attention to (i) the diversity of macro-invertebrates that prey on freshwater pulmonate snails in Africa, (ii) their suitability or unsuitability as biocontrol agents for the schistosome-transmitting snails, and (iii) the fact that both the members of the pulmonate family Physidae that have become invasive in Africa successfully avoid some of these predators. Glossiphoniidae — leeches Many leeches are predaceous and prey on a variety of benthic invertebrates, particularly oligochaetes, chironomid larvae and molluscs (Sawyer 1986). Numerous authors have shown, however, that members of the Family Glossiphoniidae are largely or exclusively malacophagous,

and have identified Helobdella and Glossiphonia as genera that feed readily on pulmonates (e.g. Michelson 1957, Harry and Aldrich 1958, Crewe and Cowper 1973, Davies et al. 1997). There is, in fact, evidence (Sawyer 1986) that glossiphoniid leeches may also be able to follow a snail’s mucus trail if they find one. The genus Helobdella is well represented in Africa, but Glossiphonia is not known from the continent (Oosthuizen and Siddall 2002). Young and Proctor (1986) showed the European Helobdella stagnalis to feed extensively on snails and Wilken and Appleton (1991) and Davies et al. (1997) showed the same for the African H. conifera. The latter species is opportunistically molluscivorous with leech-mediated leech/snail encounters occurring on a random basis. However Wilken and Appleton (1991) found, by observing responses to H. conifera-conditioned water introduced nearby with a pipette, that invasive physids, especially Aplexa marmorata, were better able to detect the predator before contact was made than either indigenous planorbids or lymnaeids. Foraging H. conifera anchor themselves by the caudal (posterior) sucker and search for prey by means of side-toside sweeps of their extended body. This movement is particularly pronounced when local water currents are set up. If no prey is found, the leech crawls, inchworm fashion, a short distance and repeats its searching activity. Contact with snail

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prey is made by the oral (anterior) sucker. The leech then releases the more powerful caudal sucker, stretches its body and swings round to attach to the shell and dislodge the snail. Once achieved, the oral sucker searches for the shell’s aperture. These leeches are liquidosomatophagous, feeding on body fluids and liquefied tissues sucked from their prey via their proboscis. When one finds the aperture the proboscis everts and penetrates the snail’s mantle and sucks out the body fluids and tissues which are partially digested by the action of proteolytic enzymes from the salivary glands before they are ingested (Sawyer 1986). They can become extraordinarily abundant if prey is plentiful – Sawyer (1986) records a density of 68 000m–2 of substratum. Helobdella conifera occurs throughout Africa and feeds readily on pulmonate snails, though it has been seen to feed on other invertebrates as well. Laboratory observations on South African H. conifera feeding on the exotic (but not invasive) Helisoma duryi (Planorbidae) (Davies et al. 1997) showed that young leeches do not feed for the first 11 days of their lives but eat between 26 and 60 snails during the rest of their lifespan of approximately 280 days. Thus they killed between 0.09 and 0.21 snails/day. The species showed a definite size-preference in prey selection, killing juvenile snails of 4–10mm diameter far more often than larger specimens. As far as prey specificity is concerned, Wilken and Appleton (1991) demonstrated that H. conifera was far more successful at killing indigenous Bulinus tropicus (Planorbidae) and Lymnaea natalensis (Lymnaeidae) than introduced Physa acuta and Aplexa marmorata (Physidae). This is because physids are able to execute escape manoeuvres in response to attack by certain slow-moving predators including leeches (see section on Predator avoidance below). Sciomyzidae — marsh flies The larvae of the marsh flies, Family Sciomyzidae, are aquatic and feed exclusively on molluscs, chiefly aquatic pulmonate snails, ripping open the prey’s haemocoel with their mouth hooks (Figure 1). Consequently they have been proposed as snail biocontrol agents in anti-schistosomiasis programmes (e.g. Berg 1953). Until the 1980s, however, little was known of the biology of African Sciomyzidae but studies by Barraclough (1983, 1985), Maharaj (1991), Maharaj et al. (1992), Appleton et al. (1993) and Miller (1995) have contributed to local knowledge of this family. These studies, all carried out in the Pietermaritzburg area of KwaZulu-Natal, South Africa (±800m altitude), showed that two of the six species occurring there can be reared easily. These two, Sepedon neavei and S. scapularis, have now been well-studied both in the field and laboratory. According to Miller (1995), S. scapularis is synonymous with S. jonesi, and is one of the most widespread sciomyzid species in Africa. Sampling of adult flies by Kitto (1991) showed that different species of Sepedon were numerically dominant in different habitats but could not identify individual species-preferences in terms of either habitat type or vegetation. He did, however, confirm the observation by Berg and Knutson (1978) that adults rest preferentially on emergent monoc-

Appleton, Hofkin and Baijnath

toyledons, mostly grasses (e.g. Leersia hexandra, Themeda triandra, Paspalum spp.) and sedges (e.g. Cyperus pulcher, Schoenoplectus corymbosus) that provide perches and oviposition sites between ±20cm and 1m above the water in which snails live. Tscheuschner (1992) extended work on adult sciomyzid distribution by showing a close correlation (r = 0.965, p < 0.05, n = 4) between the relative abundance of Sepedon (six co-existing species) and indigenous mollusc species-richness at a series of lentic and slowly-flowing habitats representing different levels of disturbance. Adult flies were most abundant at pristine sites as reflected by the number of indigenous mollusc species present. Tscheuschner’s 1992 study also described subtle differences in the foraging behaviour of S. neavei and S. scapularis larvae, the former using a passive ambushing tactic and the latter a more active searching strategy. The actual mode of attack on lymnaeid and planorbid snails by S. neavei larvae was described in detail by Barraclough (1983). Predator/prey interactions between S. neavei and S. scapularis and several exotic pulmonate species have been characterised by Maharaj (1991), Maharaj et al. (1992) and Appleton et al. (1993). The larvae of these Sepedon spp. have so far been shown to feed on 10 species of pulmonate snails: Lymnaeidae (2), Planorbidae (6) and Physidae (2). They are, like the waterbug Appasus grassei discussed below, specific in terms of prey-size but not in respect of prey-species. Smaller instars feed preferentially on smaller snails while later instars feed on snails of all sizes. During their life-cycles, individual larvae of the two fly species (S. neavei and S. scapularis) each killed 28.9–35.0 snails or 1.3–4.4/day for 8–12 days. Late (3rd) instar larvae frequently broke the shells of their prey during

Figure 1: 3rd instar larva of Sepedon neavei attacking adult Biomphalaria pfeifferi (photo R Maharaj)

African Journal of Aquatic Science 2004: 185–193

attack, as was reported for hydrophilid larvae (Coleoptera) by Maillard (1971). Importantly, all three invasive snail species exposed to sciomyzid predation, A. marmorata, P. acuta (Physidae) and L. columella (Lymnaeidae), were killed significantly less often than the indigenous species. For the two physids, this is due to the well-documented avoidance or escape reactions by the snails (see below), but for L. columella it is due to the rapid secretion of a large quantity of mucus from the footsole (Tseuschner 1992). Similar modes of attack on L. columella were observed for S. neavei and S. scapularis as follows: when a larva encounters a snail, its head usually makes contact with the snail’s foot but may not attack immediately, probing the snail instead. After contact is made, the snail extends its foot, using the footsole to fend off the larva and, as it does so, wraps the foot around the larva holding it several millimetres from the shell and immobilising it in mucus. The snail then moves away from the entangled larva which is only able to free itself after the mucus has degraded. Histological sections of the footsole of L. columella and Bulinus africanus (which produced much less mucus when attacked than did L. columella) stained in Alcian Blue showed that in both species most mucus-producing cells were in the anterior part of the sole but in L. columella these cells were situated closer to the epidermis (mean duct length 23.6µm) than in B. africanus (mean duct length 157µm). Lymnaea columella thus seems able to produce sufficient mucus to entangle an attacking larva more quickly than B. africanus. At the same time it extends its foot to keep the larva away from the shell thereby preventing it from getting its mouth hooks underneath the lip and attacking the mantle. The association between adult Sepedon diversity and habitat disturbance or modification (Tscheuschner 1992) (see above) also has implications for the control of schistosome-transmitting snails. Since adult flies require low overhanging vegetation for resting and oviposition, it is arguable that because human schistosomes are usually transmitted at disturbed sites where such vegetation has generally been destroyed either by human or stock activity, predation by sciomyzid larvae on snails is likely to be less than optimal and probably ineffective as a method of control. Belostomatidae — Waterbugs The classic work on snail predation by waterbugs (Hemiptera: Heteroptera: Belostomatidae) was done in Egypt by J Voelker in the 1960s using the giant waterbug Limnogeton fieberi (Voelker 1966, 1968). This species grows to 4–5cm, has a pan-African distribution and is, in contrast to other members of the family (see Appasus grassei below), an obligatory snail-feeder. It has five instars all of which feed on both prosobranch and pulmonate snails. For pulmonates, Voelker (1966, 1968) showed that instars I–V killed progressively more Biomphalaria alexandrina (I = 3.2, II = 5.0, III = 8.5, IV = 17.9, V = 30.0 snails/instar) but that there was no such relationship with P. acuta. In terms of daily kills, instars I–V inclusive killed between 1.8 and 2.9 (mean 2.3) B. alexandrina/day and between 1.1 and 2.0 (mean 1.6) P. acuta/day. The period of larval development was approximately 48 days but since the bugs do not feed for a day or two either side of each moult, the true figure

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should be lower. Nevertheless, if we consider the life-span of the adult bug to be about one year, this represents a considerable number of snail prey. It is noteworthy that P. acuta was unable to avoid being caught by L. fieberi (see below). Predation by Appasus grassei Formerly known as Diplonychus grassei, but transferred to the genus Appasus by Polhemus (1995), this bug measures up to 15mm and, like L. fieberi, is indigenous to Africa. Appasus grassei adults and instars III–V were shown experimentally to feed on all three snail species offered, Bulinus tropicus, Physa acuta and Aplexa marmorata (Baijnath 1999). There was no evidence of prey-specificity and they preyed effectively on indigenous planorbids (B. tropicus) and invasive physids (P. acuta and A. marmorata) alike. Methods Observations on the foraging behaviour of A. grassei and its instars that had been starved for 12h were made in 4 x 10l glass tanks each with four snails, two each (1 < 6mm and 1 > 6mm) of B. tropicus and P. acuta in Trial 1 and of B. tropicus and A. marmorata in Trial 2. Records were kept of (i) physical contact between predator and prey and (ii) attacks on snails resulting in kills. A ‘contact’ was defined as ‘grasping the prey for 5s or longer’. Dead snails were removed daily but not replaced. Separate trials were run for adults and instars and each was monitored continuously for 24h under a 10:14 dark:light regime at 21–24°C. Two replicates of each were carried out and adults were not sexed. Tanks were filled with filtered pond water. Prey specificity was analysed using the Wilcoxon Matched Pairs Signed-Ranks Test, prey size susceptibility with the G-test and avoidance responses with the Mann-Whitney U test. Results Table 1 shows that although A. grassei adults and instars II–V made similar numbers of contacts with B. tropicus and P. acuta in Trial 1 and with B. tropicus and A. marmorata in Trial 2, significantly more were made by adult bugs, followed by instars V–II in that order in both trials. Instars I and II did not kill any snails, though instar IIs did make contact with them. Instar I did not make contact with snails. There was

Table 1: Proportions (%) of total contacts made by A. grassei adults and instars II–V with indigenous (B. tropicus) and invasive snails (P. acuta and A. marmorata) in Trials 1 (n = 166 observations) and 2 (n = 660 observations. Wilcoxon Signed Ranks Test p values are given for each trial (insufficient data were available for instar II in Trial 1) Adults Trial 1 B. tropicus P. acuta p value Trial 2 B. tropicus A. marmorata p value

Instar V

Instar IV Instar III Instar II

42.0 22.2 14.8 17.3 49.4 23.5 11.8 12.9 0.2733 0.2733 0.8539 0.2850

3.7 2.4 –

73.4 9.1 11.8 70.7 10.3 13.9 0.7798 0.6858 0.5930

1.7 1.9 0.6547

4.0 3.2 0.1797

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thus no evidence that A. grassei adults and instars II–V made contact selectively with any of the available snail species (p = 0.4214 for Trial 1; 0.5786 for Trial 2). Relatively few contacts resulted in kills. Eight kills (4 B. tropicus and 4 P. acuta) were recorded in Trial 1 and 20 (11 B. tropicus and 9 A. marmorata) in Trial 2 (Table 2). Mode of attack Foraging bugs ‘hung’ nearly vertically in the water from the surface or from submerged plants, holding their raptorial forelegs ready to grasp or, more commonly, chase passing prey. On encountering a snail, A. grassei attacked it either from in front or from behind. No bugs were seen to adopt a passive strategy like the ambushing recorded for sciomyzid fly larvae (Appleton et al. 1993). Once captured the prey was securely held by the bug’s forelegs (Figure 2) and the mouthparts were inserted into the shell’s aperture and the maxillae were used to suck out the liquefied soft parts. Even while feeding, some adult bugs were seen to capture a second snail with their hind legs and hold on to it! Unlike the sciomyzid larvae (Appleton et al. 1993), A. grassei was never observed to break the shells of its prey to gain access to the soft parts and, since neither Voelker (1966, 1968) nor Raut and Saha (1989) commented on this, it seems that foraging Belostomatidae do not damage their victims’ shells. A feature of the feeding behaviour of these waterbugs (also H. conifera and Sepedon larvae) was their partial consumption of prey – they seldom consumed all of the soft parts of their prey and in some cases ate very little. Appasus grassei does not appear to exhibit speciesselectivity in killing its prey (G = 1.5899, 0.05 < p > 0.90 for Trial 1; G = 2.01476, 0.05 < p > 0.5 for Trial 2). No instar II were seen to kill snails although, as shown in Table 1, they did make contact with them. It was estimated from Table 2 that adults could each kill 6.5 snails (not necessarily of the same species) per 24h period, instar V 2.0, instar IV 4.5 and instar III 1.0 snails/24h. However this is probably an over-estimate because adults were observed to feed on a single snail for several hours (and on one occasion for 24 hours) and A. grassei kills and feeds on other invertebrates as well. No prey preference trials were done on other invertebrate taxa. Data on prey size susceptibility showed that similar numbers of small (6mm) snails of each species were killed in each trial, regardless of whether the predator was an adult or an instar. Contrary to the findings of Raut and Saha (1989) for the Indian belostomatid S. annulatum, A. grassei did not exhibit any significant size

preference in selecting its prey and instars III–V as well as adults killed snails in both size classes, 80% of snails left the water within 15 minutes (and often within 5 minutes), generally crawling out to a distance of at least 1.5cm above the water level, and occasionally as far as 6cm. If pushed back into the water, the snails quickly crawled out again but stayed submerged if placed in a tank without P. clarkii. Of the three snails that did not crawl out, two were eaten by P. clarkii and the third was alive when the observations stopped. Less than 20% of snails in experiments 2 and 3 left the water during the observation period. It thus appears that P. acuta avoids predation by P. clarkii through the simple expediency of leaving the water, rather than using the range of ‘avoidance manoeuvres’ reported for encounters with slow-moving predators such as H. conifera and Sepedon spp. But physids are versatile snails and it has been demon-


80 70 60 50 40 30 20 10 0

1

2

3

4

5

6

Instar II Instar III Instar IV Instar V Adult

(c)

100 90 80 70 60 50 40 30 20 10 0

1

2 3 4 5 RESPONSE TYPES

6

Instar II Instar III Instar IV Instar V Adult

Figure 3: Frequencies (%) of avoidance response types 1–6 (as defined by Wilken and Appleton 1991) elicited from (A) the indigenous snail B. tropicus, (B) P. acuta and (C) A. marmorata after encounters with A. grassei


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strated (Crowl and Covich 1990) that at least one North American species, Physella virgata, displays phenotypic plasticity when exposed to predation pressure by modifying its life history. Faced with attacks by the crayfish Orconectes virilis, a predator that preys mostly on the smallest snails, P. virgata postpones the onset of its maturity until it has reached a size larger than the predator’s preferred prey-size range. This effectively reduces the effects of predation, and other physids may be also be expected to employ this tactic. Potential as biocontrol agents There is no evidence that any of the predator taxa discussed above are prey specific at the species, genus or even family level. Because of this lack of prey specificity, they should all be expected to feed on any indigenous pulmonates encountered and, except for Sepedon spp. and possibly H. conifera, on other macro-invertebrates as well. Biological control of medically important snails (Lymnaea, Biomphalaria and Bulinus spp.) will therefore require the mass release of reared predators into the targeted habitats — ‘biocontrol by predator augmentation’. When present at high densities, these predators may play a role in regulating the populations of their snail prey. Sepedon neavei larvae were tested in quasi-field trials but had no observable effect on snail populations (Appleton et al. 1993). In fact, neither S. neavei nor S. scapularis larvae are considered suitable for the biological control of the schistosome-transmitting snails because, being airbreathers, they need to have regular access to atmospheric oxygen and so keep their posteriorly-situated spiracles at the surface. To achieve this, the larvae are kept buoyant by an air bubble in the gut and do not forage effectively at depths of more than a few centimetres. Indeed, if the weight of a snail captured close to the surface causes the larva to sink, it will release the snail and float back to the surface. When submerged, their spiracles are closed by specialised fleshy lobes.

Although no control trials have been carried out with belostomatids, Pointier and Delplanque (1976) considered that Belostoma boscii could play a role in the regulation of Biomphalaria glabrata populations in Guadeloupe and Dillon (2001) proposed that the North American Belostoma flumineum was able, under certain conditions, to exert ‘meaningful predation pressure on physid populations’. Reviewing studies on predation of the North American Physa vernalis by B. flumineum, Dillon (2001) noted that predation rates varied with bug size, from 1.8 snails/bug/day for 4.5mm immatures (instar not recorded) to 3.5 and 5.5 snails/bug/day for adult males and females respectively. He proposed that these rates were higher than those achieved by B. flumineum in the field, which were probably closer 0.5 snail/bug/day. Belostoma flumineum is a larger species than A. grassei but both are generalist feeders which forage opportunistically so that bug/snail encounters will depend on both snail density and the predator’s life cycle. These constraints will also apply to the probably excessively high predation rates measured in the laboratory for other predators (see Table 4). Recently Aditya and Raut (2001) proposed that Sphaerodema rusticum, which is also malacophagous, be used to control P. acuta, which has become a problem in sewage works in India. Procambarus clarkii, the only exotic species reviewed here, has been shown, by default rather than by design, to be an efficient predator of the snails serving as intermediate hosts for human schistosomes to the extent that it reduced transmission in certain types of habitat in east Africa (Hofkin et al. 1992, Mkoji et al. 1999). Its success as a biocontrol agent will undoubtedly result in calls for its introduction to other endemic areas. However, as pointed out by Hart (1983), Van Eeden et al. (1983) and Mikkola (1996), it is an invasive species and must be considered an undesirable immigrant with the potential to cause environmental damage. Proposals to introduce it for control purposes will therefore involve interesting ethical debate! No practical experiences are available to assess the value of either glossi-

Table 3: Numbers of P. acuta leaving the water or staying submerged after exposure to (1) live P. clarkii, (2) P. clarkii-conditioned water and (3) clean water (control) (n = 16) Experiment 1. P. acuta + P. clarkii 2. P. acuta + crayfish-conditioned water 3. P. acuta + fresh water

No. crawling out (%) 13 (81.25) 1 (6.25) 3 (18.75)

No. staying submerged (%) 3 (18.75) 15 (93.75) 13 (81.25)

Table 4: Some predation characteristics of the predators reviewed in the text Predator

Malacophagous stages

Helobdella conifera Sepedon spp. Limnogeton fieberi Appasus grassei Procambarus clarkii

juveniles and adults all instars all instars instars III–V probably all stages

Potamonautes spp.

Laboratory estimation of no. snails killed during predator’s lifetime

26–60 29–35 ±500 ±1 277 50–100/48h depending on larval stage adults (no data on juveniles) not known

Preys on indigenous and/or exotic snails

Source

Indigenous Davies et al. 1997 Indigenous Maharaj 1991 Both Voelker 1966, 1968; Baijnath 1999 Both Indigenous (no data Hofkin et al. 1991; B Hofkin unpubl. on exotics) data; G Gouws pers. comm. Probably both

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phoniid leeches or river crabs as biocontrol agents, and further research on these taxa is needed. Acknowledgements — Patrick Reavell (University of Zululand) kindly identified Appasus grassei and Dra E Naranjo-García (UNAM, Mexico) commented on a draft of the manuscript.

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