Regulatory Influence of Procambarusclarkii,
Girad (Decapoda: Cambaridae) On
Schistosome-Transmitting Snails in Lotic
Habitats within the River Athi Basin, Kenya
Maina GM1,3*, Kinuthia JM1, Mutuku MW1, Mwangi IN1, Agola EL1, Kutima HL2 and
1Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya
2Department of Zoology, Jomo Kenyatta University College of Agriculture and Technology, Juja, Kenya
3College of Health Sciences, Institute of Tropical Medicine and Infectious Diseases (ITROMID), Jomo
Kenyatta University of Agriculture and Technology, Juja, Kenya
Maina GM, Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, Kenya, Tel:
+254720 999 586; E-mail:
Received: September 21, 2017; Accepted: October 05, 2017; Published: October 11, 2017
Maina GM, Kinuthia JM, Mutuku MW, Mwangi IN, Agola EL, Mkoji GM, Kutima HL (2017) Regulatory Influence of
Procambarusclarkii, Girad (Decapoda: Cambaridae) On Schistosome-Transmitting Snails in Lotic Habitats within the River Athi
Basin, Kenya. Int J Marine Biol Res 2(1): 1-7. DOI: 10.15226/24754706/2/1/00113
Background & Objective: Control of schistosomiasis, a neglected tropical disease has for a long time overly relied on praziquantel. Crayfish, though voracious snail eaters have been tested in small man-made impoundments but not in lotic habitats. The present study aimed to determine the ability of the crayfish, Procambarusclarkii to reduce populations of schistosome transmitting snails in lotic habitats.
Methods: Data was collected bi-monthly on the presence or absence of snails and crayfish in4 stream habitats, over a period of 10 months, and
these were identified from a baseline survey to be habitats for Biomphalaria snails, transmitters of intestinal schistosomiasis, and were located in
the Machakos County within the Athi River basin in south-eastern Kenya. Subsequently, 2 of the habitats were selected for introduction of crayfish
(and were designated “experimental sites”) and the other 2 habitats were designated “control sites.” Each of the “experimental sites” received 110
crayfish. The study sites were sampled for snails using standard snail scoops and for crayfish using meat-baited crayfish traps. The bi-monthly
sampling of the habitats was done to determine snail abundance, crayfish survival, and obtain information on biotic and abiotic parameters.
Results: Snail abundance in the habitats that received crayfish rapidly declined within 2 months to a significant level compared with the initial abundance (paired t test = 5.524, p value = 0.0001), relative to the decline observed in the control habitats (paired t test = 7.727, p value = 0.082).
Interpretation & Conclusion: While P.clarkiiholds much promise as a complimentary schistosomiasis control strategy to chemotherapy,
restocking of habitats should be considered when habitats dry up during extreme weather conditions, for effectiveness of this approach.
Keywords: Crayfish; Predation; Planorbid snails; Biomphalariapfeifferi; Seasonal streams; Schistosomamansoni
Schistosomiasis is one of the several so-called neglected
tropical diseases (NTDs) that are pervasive in sub-Saharan Africa
and elsewhere in the developing world . Various strategies for
control include chemotherapy to treat infected people, improved
sanitation, public health education programs, and snail control
. Today, public health campaigns in endemic regions focus
on mass drug administration using the oral drug, praziquantel
(PZQ) . Although PZQ is fairly efficacious against the sexually
mature forms of the parasite, it is often unable to kill juvenile
schistosomes present in the human body . Additionally, there
is concern that with the intensive use of PZQ drug resistance
could render PZQ ineffective; given that drug resistant strains
can easily be selected in the laboratory  and field derived
strains with reduced susceptibility have been described .
Although artemether is known to be effective against immature
schistosomes in the definitive host6and since most of the
schistosomiasis endemic areas are also endemic for malaria
transmission, there is reluctance to use it in such areas for fear of
emergence artemether resistance . Efforts to control the snail
populations in the past through the use of chemicals or through
alteration of snail habitats have resulted in environmental
pollution and damage . Another shortcoming associated with
chemotherapy is that continued re-exposure to cercarial infested
water leads to rapid re-infections of successfully treated patients
in the endemic areas [9,10,11].
Biological control of schistosomiasis as a complimentary
strategy to existing control strategies is not commonly used in
control programs primarily because it may involve use of exotic
species which may negatively impact the local environment,
possibly leading to extinction of the native bio-diversity .
However, studies carried out on fresh water snails in the
Neotropical area have shown that the invading species may
have a positive influence from the human health point of view,
if their introduction leads to displacement of snail species
that are responsible for the transmission of schistosomiasis
. The case of Martinique Island is especially relevant as a
successful bio-control strategy where Biomphalariaglabrata
and Biomphalariastraminea were displaced by the thiariid,
Melanoidestuberculata after its accidental introduction
into this island [14, 15]. A bacterial pathogen of snails,
Paenibacillusglabratella, has also, been tested on B. glabrata. The
bacterium causes massive mortality and affects both the adult
and neonate snails . However, it is unclear at this point; if
the bacterium is specifically infective to the snails that serve as
intermediate hosts for schistosomes, or it can also, infect other
invertebrate species. A river prawn, Macrobrachiumvollenhovenii,
has also, been tested with varying success in River Senegal, Diama
Dam, using the male prawns .
The red swamp crayfish, Procambarusclarkii, α native of
South-Central United States and North-Eastern Mexico, has been
introduced to Europe, Africa, Central and South America and
South-East Asia . It was introduced into Lake Naivasha in
Rift Valley, Kenya in the 1970’s, and has since spread throughout
several parts of Kenya. Previous studies indicated that P. Clarkiiis
an effective predator of snails , rapidly eliminated snail
populations in small man-made ponds , and, effectively
reduced schistosomiasis transmission in such habitats .
However, no studies have been done in seasonal stream habitats
which also, form significant foci for schistosomiasis transmission
in endemic areas such as Kenya. In the present study, P. clarkii
was tested for its ability to eliminate Biomphalariapfeiferi, the
freshwater snails involved in the transmission of S. mansoniin
stream habitats located in the Machakos County, within the River
Materials and Methods
This study received approval from the Kenya Medical Research
Institute (KEMRI) through its Scientific and Ethical Review Unit
(SERU) and is referenced SSC No. 2798. Permission to undertake
this study was also, obtained from the Kenya Wildlife Services
(in a letter referenced KWS/BRM/5001) and the National
Environment Management Authority (NEMA/10/22/VOL.1). The
purpose of the study was explained to the local community in
both the Kiswahili language and in the local Kikamba language,
particularly to the people that lived near or frequently utilized
the study habitats.
Latex rubber gloves were worn by the project staff during snail
sampling to prevent accidental exposure to schistosomecercariae, while heavy duty leather
gloves were worn to prevent accidental crayfish bites during sampling.
The study was undertaken in the Machakos County of Kenya, in
localities within the River Athi Basin, in seasonal streams, identified
through an initial survey as habitats for Biomphalariapfeifferi, a
prominent snail host of Schistosomamansoni, the causal agent of
Baseline Survey and Data Collection
Out of the 15 stream habitats surveyed in the area, 4 were
selected as the study habitats, and were sampled bi-monthly
between June 2014 and March 2016. Two of the 4 selected study
stream habitats (namely Kyanguli and KwaMutanga streams)
were designated “Experimental” and received crayfish after an
initial 6-months baseline sampling. The other 2 (Kyaana and
Kamuongo) were designated as “Control” and no crayfish were
introduced into the habitats. All the 4 study habitats selected had
thriving populations of B. Pfeifferisnails which persisted for the
6 months all the habitats were sampled, prior to the introduction
of crayfish into the “Experimental” sites. In each study habitat, 3
sampling stations were identified and marked, and were sampled
during each visit to the habitats. The study habitats were sampled
to determine presence or absence of crayfish, snail and crayfish
abundance, and to determine schistosome infection prevalence in
the snail populations.
Snail Sampling and Screening
Snails were sampled in all the 4 study habitats at designated
sampling stations using standard snail scoops made of stainless
steel sieves with a mesh size of 2×2 mm, supported on an iron
frame, and mounted on a 1.5 m long wooden handle. Snails were
sampled for 15 min at each sampling station along the littoral
zones. Sampling was done between 0900 hrs and 1230 hrs. The
snails collected were sorted into species, counted, and screened
for mammalian schistosome infections. Screening for schistosome
infections was done using the “shedding” method in which the
snails are isolated individually into wells of 24-well culture plates
in 1 ml of mineral or aerated water, and left under natural or
artificial light for 1.5-2hr to induce release of the schistosome
larval forms known as cercariae, which develop in the snails and
are infective to humans and other susceptible mammalian hosts.
Crayfish were sampled using locally made traps of plain wire
and onion bags as shown in (Figure 1). The wire was cut into
several 45 cm pieces. Where 3 pieces were folded to form circles
and welded at the joints. Three straight wires were running the
length of the three circles at equal distances and riveted at each
point of contact with the circular wires. The traps were randomly
placed in the water, and left for a maximum of 1hr, but were
checked at 15 min intervals. Any crayfish caught were removed
from the traps and placed in a lidded plastic bucket. The captured
crayfish were then sized, sexed, counted, and then returned
into the water after sampling. Only male catches were analyzed
because they provided the best index of crayfish abundance .
Figure 1: A photograph of trapped crayfish taken at Kyanguli stream
(Experimental) where the crustaceans established thriving populations
leading to decimation of snails.
Figure 2: Juvenile crayfish
The Study Habitats
The streams discharge is highly seasonal with peak flow in
April-May when flooding is sometime observed and scanty flow
in December-February. The streams bed is very variable ranging
from rocky bed, large blocks (> 1m), stones (5-25cm), coarse
and fine gravel (2-50mm), and sand (< 2 mm) with fine organic
matter in small pools. Both emergent and sub-mergent aquatic
macrophytes occur. Most of the streams habitats are still kept in
natural status save for sand harvesting and small scale irrigation.
Anthropogenic activities in these streams include but not limited
to; clothes washing, bathing, watering domestic animals, fetching
water for domestic use, manual and mechanized small scale
Snail Species Present in the Study Habitats
Several snail species inhabit the streams including B. pfeifferi,
B. nasutus, B. forskalii, Ceratophalus and Lymneanatalensis. A
total of 2325 schistosome transmitting snails (B. pfeifferiand
B. nasutus) were sampled during the September 2014-March
2016 in the 4 study streams. The number of the other species
sampled was small with B. forskaliiat 17, Lymneanatalensis125
and Ceratophalusat 23.
Crayfish Performance in the New Habitats
Following crayfish introduction in Kyanguli and KwaMutanga
streams, the crayfish were able to establish thriving populations
at Kyanguli. During the 20 month period of the survey, 6 juvenile
crayfish, an indication of breeding, were spotted on the edges
of the experimental streams. 77 adult predators were captured
in Kyanguli stream over the entire study duration while 28
adult crayfish in Kwamutanga within the first 3 months post
introduction. (Figure 3) shows juvenile crayfish captured at
Figure 3: KwaMutanga stream, a motor cycle taxi (Bodaboda) washing
site, and where crayfish failed to survive or establish a population, after
Snail Abundance in the Study Habitats
After introduction of the crayfish in the “Experimental”
habitats, a rapid decline in snail abundance was observed.
For instance, within 3 months of crayfish introduction, snails
completely disappeared at Kyanguli stream, never came back
during the next 12 months of sampling at this habitat. At
KwaMutanga stream, the snail abundance declined rapidly as well
within 2 months of crayfish introduction (Figure 6). However,
crayfish had rarely established at this site due to human activities
specifically cleaning of motor bikes (Figure 3). On the other hand,
snails remained relatively abundant in the “Control” habitats
(Kyaana and Kamuongo streams), even though the numbers
fluctuated over time, during the observation period, snails never
completely disappeared from these habitats (Figure 7).
The population of snails sampled was more in experimental
streams than in control stream. This could be attributed to the
accuracy of the sampling method or even natural variation of the
population density due to breeding or even habitat suitability.
However, the population in control streams grew to almost same
levels as in experimental streams by January 2015 just before
crayfish was introduced. This provides a basis to evaluate the
effect of crayfish on snail population density that would be used
as potential biological control for schistosomiasis.
Figure 4: Snail abundance in experimental streams before Crayfish introduction
Figure 5: Snail abundance in Control streams before crayfish was introduced
in experimental streams
Figure 6: Snail abundance after crayfish introduction (Experimental)
Figure 7: Snail abundance in control streams over the study period
The snail population in experimental streams was significantly
reduced (paired t test = 5.524, p value = 0.0001) compared to
control streams (paired t test = 7.727, p value = 0.082) after the
crayfish was introduced. This indicates that the crayfish was able
to establish in the habitat and feed on snail as one of their source
if nutrients for survival.
Comparison of Experimental and Control snail
abundance after crayfish introduction
Kwamutanga stream (Figure 8) the crayfish temporarily
established within the first 3 months post introduction, almost
wiped out the snails, but the crayfish pettered out by the 4th
month leading to a resurgent of snails, may be due to the stream
being used for motorcycle taxi washing. However, in Kyaana
stream (control) snail population declined from January 2015
till May due to drying of the river and then increased during
the months of June and July 2015 (Figure 9). A slight decrease
was observed during August as water levels declined and then a
steady population reached from November 2015 through March
2016 in Kyaana stream. A comparison using one sample t test
showed a significant difference (t = 10.575, p = 0.0001). This
shows despite environmental changes such as flooding, drying
and human activity, crayfish fed on snail leading to a significant
drop in their population.
Figure 8: Snail population decline in KwaMutanga after crayfish introduction
compared to Kyaana control stream
Figure 9: Snail population in Kyanguli after crayfish introduction compared
to Kamuongo control stream
A comparison using one sample t test shows significant
difference (t = 4.651, p = 0.001) of snail population between the
two streams after crayfish was introduced in Kyanguli stream.
Even though snail population was affected by environmental
factors in Kamuongo stream, the same was also experienced in
Kyanguli but the total decline was attributed to the predators
(crayfish) introduction. The snail population in Kyanguli stream
declined drastically from March 2015 and was totally eliminated
by July 2015 through March 2016.
Table 1: Snail population pre and post introduction of Crayfish
Snail Abundance Before Crayfish Introduction
Snail Abundance After Crayfish Introduction
Statistical Analysis by Paired t-Test
This study is the first attempt to determine the effect of
crayfish on snail populations in stream habitats. Previous studies
in small man-made ponds located within the Athi river Basin in
Kenya showed that crayfish rapidly reduced snail numbers in
such habitats, and indeed, in one stable habitat, they established
self-sustaining populations and prevented re-establishment of
snails for several months . In the present study the effect
of crayfish on pulmonate snail populations was determined in
stream habitats. While crayfish are known to occur in stream
habitats in Kenya, their ability to eliminate pulmonate snails of
medical and veterinary significance in the country has not been
determined. The fact that crayfish were able to persist at Kyanguli
over several months and eliminated the snail populations in this
habitat suggest that P. clarkii could play a role in control of snails
of medical or veterinary significance in endemic areas such as
Kenya. Although KwaMutanga stream seemed an ideal habitat
for crayfish establishment, we experienced difficulties getting
the crayfish to survive or establish in this habitat. While we
do not have an explanation why crayfish could not establish in
this habitat, we suspect pollutants that could potential kill the
crayfish may have present in the stream. Apparently, the site
at which we released the crayfish into the habitat is frequently
used as a motorcycle taxis (locally popularly known bodaboda)
washing site, and it is possible that petroleum products from the
motor cycles such as oil or petrol may be responsible for failure of
crayfish to survive and establish at this site.
Bio-control means for control of snails of medical or
veterinary importance is preferred to chemical mollusciding,
as it is not only considered environment friendly but also offers
sustainability . As schistosomiasis is transmitted from water
sources frequent use of chemical molluscicides may have longterm
adverse affects on water ecosystem as well as negatively
affect people and animals that use the same water sources. In the
search, for effective biological control agents against schistosometransmitting
snails, the crayfish appears to be particularly
promising given that it is an efficient predator of pulmonate
snails responsible for transmitting disease causing parasites in
both humans and livestock . However, it is envisaged that the
widespread use of this crustacean for snail control will most likely
be based on continual or repeated restocking of the predator in
the transmission sites analogous to the use of molluscicides as
transmission sites of such parasites include seasonal streams
which are subject to frequent flooding during heavy rains, which
end up washing away the crayfish, or to drying out completely
in the dry season which may lead to the disappearance of the
In the current study, though adult crayfish were recovered in
Kyanguli stream on subsequent bi-monthly sampling, it was not
possible to tell whether the catches represented the originally
introduced crayfish or their progenies, future studies should seek
to uniquely tag the released crayfish to differentiate them from
F1 and subsequent generations. The researchers recommend
further work to establish the feasibility of the use of crayfish as
biocontrol of schistosomiasis.
Although this study was limited by the number of study
habitats, study duration, and also, experienced setbacks with
flooding and in one habitat, possible human-related interference
which, overall may have influenced the outcome of this study,
the data obtained demonstrates the potential of the decapod
crustacean, Procambarus clarkia, as a biological control agents
against aquatic snails responsible for transmission of trematode
parasites that cause disease in humans and domestic livestock,
such as schistosomiasis (bilharzias) and fascioliasis (liver fluke
disease) in stream habitats which may sometimes experience
flooding or long dry season, and therefore, may require restocking
or re-introductions, once in a while. Further studies
on this crustacean should therefore, be encouraged. The study
limitation included environmental factors such as floods, drought
and human activity affected survival of the snails and thus
limits generalization of the results. The snail survival in both
experimental and control streams were negatively affected by
flooding and human activity such as washing of motorbikes which
would reduce the impact of the intervention strategy applied
in this study. However, there is a clear indication that crayfish
had significant impact to the decrease of the snail population
in the experimental streams. This environmental impact would
be reduced by replicating the study in artificial setting such as a
swimming pool where most variables can be controlled.
Conflict Of Interest
Authors declared no conflict of interest
This research was funded through an Internal Research
Grant (IRG) from the Kenya Medical Research Institute (KEMRI),
referenced (PJ-611). We thank the communities that live near
the study sites for their support and cooperation. We appreciate
Messrs. Stephen Kamau and Newton Mwathi who supported field
data collection. This paper is published with the approval of the
Director, Kenya Medical Research Institute (KEMRI).
- World Health Organization.http://www.who.int/mediacentre/factsheets/fs115/en/2014.
- Inobaya MT, Olveda RM, Chau TN, Olveda DU, Ross AG. Prevention and control of schistosomiasis: a current perspective. Res Rep Trop Med. 2014;5:65-75.
- Pica-Mattoccia L, Cioli D. Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. Int J Parasitol. 2004;34(4):527–533.
- Aragon AD, Imani RA, Blackburn VR, Cupit PM, Melman SD, Goronga T, et al. Towards an understanding of the mechanism of action of praziquantel. Mol Biochem Parasitol. 2009;164(1):57–65.
- Fallon PG, Doenhoff MJ. Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am J Trop Med Hyg. 1994;51(1):83–88.
- Steinauer ML, Melman SD, Cunningham C, Kubatko LS, Mwangi IN, Wynn NB. Reduced susceptibility to praziquantel among naturally occurring Kenyan Isolates of Schistosoma mansoni. PLOS Negl Trop Dis. 2009;3(8):e504. doi:10.1371/journal.pntd.0000504
- Hala E, Marcel T, Robert N, Bergquist RN, Soraya S, Rashid B. Prophylactic effect of artemether on human Schistosomiasis mansoni among Egyptian Children: A randomized controlled trial. Acta Tropica. 2016;158:52-58.
- Utzinger J, Chollet J, Jiqing Y, Jinyan M, Tanner M, Shuhua X. Effect of combined treatment with praziquantel and artemether on Schistosoma japonicum and Schistosoma mansoni in experimentally infected animals. Acta Tropica. 2001;80(1):9-18.
- Spear RC, Seto E, Remais J, Carlton EJ, avis G, Qui D, et al. Fighting waterborne infectious diseases. Science. 2006;314(5802):1081–1083. doi:10.1126/science.314.5802.1081c
- Fenwick A, Webster JP. Schistosomiasis: challenges for control, treatment and drug resistance. Curr Opin Infect Dis. 2006;19(6):577–582.
- Tchuem Tchuenté LA, Momo SC, Stothard JR, Rollinson D. Efficacy of praziquantel reinfection patterns in single and mixed infection foci for intestinal and urogenital schistosomiasis in Cameroon. Acta Tropica. 2013;128(2):275–283.
- Secor WE. Water-based interventions for schistosomiasis control. Pathog Glob Health. 2014;108(5):246-254. doi:10.1179/2047773214Y.0000000149
- Webster BL, Diaw OT, Seye MM, Faye DS, Stothard JR, Sousa-Figueriredo JC, et al. Praziquantel treatment of school children from single and mixed infection foci of intestinal and urogenital schistosomiasis along the Senegal River Basin: Monitoring treatment success and re-infection patterns. Acta Trop. 2013;128(2):292–302. doi:10.1016/j.actatropica.2012.09.010
- Lodge DM, Deines A, Gherardi F, Yeo DCJ, Arcella T, Baldridge AK, et al. Global introductions of Crayfishes: evaluating the impact of species invasions on ecosystem services. Annu Rev Ecol Evol Syst. 2012;43:449–472.
- Prentice MA. Displacement of Biomphalaria glabrata by the snail Thiara granifera in field habitats in St. Lucia, West Indies. Ann Trop Med Parasitol.1983;77(1):51-59.
- Pointier JP. Invading freshwater gastropods: some conflicting aspects for Public health. Malacologia. 1999;41(2):403-411.
- Pointier JP. Comparison between two biological control trials of Biomphalaria glabrata in a pond in Guadeloupe, French West Indies. J Med Appl Mal. 1989;1:83-95.
- Pointier JP, Guyard A. Biological control of the snail intermediate hosts of Schistosoma mansoni in Martinique, French West Indies. Trop Med Parasitol. 1992;43(2):98-101.
- Duval D, Galinier R, Mouahid G, Toulza E, Allienne JF, Portela J, et al. A novel bacterial Pathogen of Biomphalaria glabrata: A potential weapon for Schistosomiasis Control? Plos Negl Trop Dis. 2015;9(2):e0003489. doi:10.1371/journal.pntd.0003489
- Sokolow SH, Lafferty KD, Kuris AM. Regulation of laboratory populations of Snails (Biomphalaria and Bulinus spp.)by river prawns, Macrobrachium spp. (Decapoda, palaemonidae): Implications for control of schistosomiasis. Acta Trop. 2014;132:64-74. doi:10.1016/j.actatropica.2013.12.013
- Huner JV. Freshwater Crayfish: Biology, Management and Exploitation. Edited by Holdich DM, Lowery RS. Portland: Timber Press; Procambarus in North America and elsewhere 1988;239–261.
- Loker ES, Hofkin BV, Mkoji GM, Kihara JH, Mungai B, Koech DK. Procambarus clarkia in Kenya: does it have a role to play in the control of schistosomiasis? Aquaculture and Schistosomiasis: Proceedings of a Network Meeting Held in Manila, Philippines, August 6–10, 1991. 1992; Washington, DC: National Academy Press, 272–282.
- Lodge DM, Stein RA, Brown KM, Covich AP, Brönmark C, Garvey JE, et al. Predicting impact of freshwater exotic species on native biodiversity: challenges in spatial scaling. Australian Journal of Ecology. 1998;23(1):53–67.
- Yue GH, Li JL, Wang CM, Xia JH, Wang GL, Feng JB. High prevalence of multiple paternity in the invasive crayfish species, Procambarus clarkii. Int J Biol Sci. 2010;6(1):107–115.
- Mkoji GM, Hofkin BV, Kuris AM, Stewart-Oaten A, Mungai BN, Kihara JH, et al. Impact of the crayfish, Procambarus clarkia on Schistosoma haematobium transmission in Kenya. Am J Trop Med Hyg. 1999;61(5):751–759.
- Sulieman Y, Pengsakul T, Guo Y, Huang SQ, Peng WX. Laboratory and Semi-Field Evaluation on the Biological Control of Oncomelania hupensis Snail (Gastropoda: Pomatiopsidiae), the intermediate host of Schistosoma japonicum, Using Procambarus clarkii crayfish (Crustacea: Cambaridae). Egyptian Journal of Biological Pest Control. 2013;23(1):215-220.
- Sharma A, Diwevidi VD, Sigh S, Pawar KK, Jerman M, Singh LB, et al. Biological Control and its Important in Agriculture. International Journal of Biotechnology and Bioengineering Research. 2013;4(3):175-180.