Medically Important Parasites of Clarias Garipienus (Catfish) in Nigeria
Odoh Victoria Ugbede*, Abuh Ojomona Oboro, Haruna Martha M, Yisa Michal Awawu, Bids Alhaji Audu and Zaliya Ibrahim Waziri
Department of Biological Sciences, Federal University of Technology, Nigeria
Submission: October 14, 2019; Published: December 06, 2019
*Corresponding author:Odoh Victoria Ugbede, Department of Biological Sciences, Federal University of Technology Minna-Nigerstate, Nigeria
How to cite this article: Odoh V U, Abuh O O, Haruna M M, Yisa M A, Bids A A. Medically Important Parasites of Clarias Garipienus (Catfish) in Nigeria. 0010 Adv Biotechnol Microbiol. 2019; 15(1): 555904. DOI: 10.19080/AIBM.2019.15.555904
Abstract
Parasites of Clarias gariepinus is of medical importance which affects economic value of fish produced and raised public health concern in the different geopolitical zones in Nigeria. C. gariepinus examined for both endo and ecto parasites respectively in several review work shows different parasites belonging to different groups. These include cestode, nematode, trematodes and Protozoan. Trematodes are among the major parasites found affecting C. gariepinus, it damages the muscles of fish making it disgusting and unmarketable. In human flatworm causes a condition called Trematodosis. Fish roundworms (Nematodes) causes a condition in human called Aniskiasis. Fish tapeworms(cestodes) causes a condition in human called Diphyllobothriasis. C. gariepinus has shown high parasitemia of both medical and economic concern, its high level of endoparasites and ectoparasite may result in adverse conditions either to the aquatic system or to animals (human inclusive) who consumer this species of fish..
Keywords: Clarias gariepinus, Medical important; Parasites; Docosahexaenoic acid; Eicosapentaenoic acid; Ichthyophthirius multifiliis; Trichodina spp; monogeneans; Animals; Pseudoterranova decipiens
Introduction
Fish is a cheap and important source of protein which also contains calcium, lipids, minerals, vitamins and oils with desirably low cholesterol levels in the diets of fish lovers. Economically, it is a source of income and it has continued to be the most affordable source of animal protein to an average Nigerian family [1]. The byproduct of fish can be incorporated into feeds of livestock and poultry. Fish accounts for more than 40% of the protein diet of two-thirds of the global population. Fish interacts with the various levels of food chain and influence the structures of lakes, streams and estuaries since they are usually restricted to particular modes of life related to their food sources and reproductive requirements [2].
The African catfish Clarias gariepinus belonging to the family claridae is the most popular fish food which is considered to be one of the most important tropical fish for aquaculture in Nigeria [3]. It is very common in swamps lakes and rivers throughout Africa and it is the main fish fisherman catches. C. gariepinus hold great promise in fish farming in Africa due to its wide geographical spread, high growth rate and it resistant to stress. It is well appreciated, highly priced and requested for by both fish farmers and consumers in Nigeria in either smoked or fresh form. It is found throughout Africa, Nigeria inclusive and live in freshwater and human-made habitat, such as the earthen pond or concrete ponds. The fish was introduced all over the world in the early 1980’s for acquaculture purposes [3].
Cited that in many parts of Nigeria, consumption of catfish has been regarded as part of exclusive delicacies for the upper class, although the cost is within the rich of the majority. Catfish is one of the major sources of omega-3 fatty acid, which is very important nutrient that protect the body against some of the most common deadly non communicable diseases especially cardio-vascular disease, Omega-3 fatty acid consist of Docosahexaenoic Acid(DHA) and Eicosapentaenoic acid (EPA), which are essential fatty acid that need to be supplied regularly in human diet. His work on retrospective and descriptive cross-sectional survey among 259 consenting respondent and 50 catfish farmers reflected the level of acceptability of consumption of catfish [4].
Physiology and morphology of medical important fish parasite
In his work, on Parasitic Protozoan isolated Ichthyophthirius multifiliis from skin and gills of infested C.gariepinus. The Parasiteis the largest known parasitic protozoan found on fishes. Adult organisms are oval to round and measure 0.5 to 1.0 mm in size. The adult is uniformly ciliated and contains a horseshoe-shaped nucleus which can be seen in older individuals. Trichodina spp. is isolated from skin, fins and gills of infested C.gariepinus This parasite is large with disc shaped body. The adhesive disc is saucer shaped. The parasite is provided with several rows of cilia at the circular periphery and the inner circle of toothed denticles. The macronucleus is horseshoe-shaped, and micronucleus is small and difficult to be seen in some specimens. Epistylis spp. is isolated from skin and gills of infested catfish. It is a sessile contractile ciliate. Stalk is long and noncontractile. Often forms a branched colony. The distal end of the organism is surrounded by rapidly moving cilia which appear as a blur. The monogenetic Gyrodactylus is detected in gills and skin of infested C. gariepinus. It is flat worm with one pair of projection at its anterior pole. It can be distinguished from other monogeneans by the absence of eye spots and the occurrence of the embryos in the mid-region of the body (Viviparous monogenean). Posterior end has the organ of fixation, opisthaptor, which is guarded with a number of marginal hook lets and a central one pair of hooks.
Zoonotic fish parasite
The ability of fish especially freshwater fish like Clarias gariepinus transmit parasite to human and animals is well recognized [5]. Mentioned that some parasite of fishes is zoonotic while they are also capable of serving as intermediate host or definitive host of parasites that may be harmful to man or other animals. The occurrence of this medically important parasites in C. gariepinus varies considerably from one geographical region to another and amongst fish farm. The protozoans and helminths are reported to be the major group of parasites of fish (including Clarias gariepinus) involved in parasitism in Nigeria. Endoparasite reduced fish availability for consumption and also increased the danger of fish parasites occurring in our food, which serve as a threat to human health. Parasites usually exist in equilibrium with their host as a survival strategy [6,7]. reported that a moderate number of nematodes, trematodes, cestodes and acanthocephalans infest humans, but held that only a few cause serious diseases. According to him, the most important of the helminths acquired by humans from fish are the anisakis nematodes (particularly A. simplex and Pseudoterranova decipiens), cestodes of the families Heterophylidae, Opisthorchilidae and Nanophyetidae [8]. Studied the risk of infection with fish-borne parasites and mention that they present a potential threat to the health of human consumers. Parasites like tapeworm species that occur in fish can infect people and other fish-eating mammals, if they swallow living larvae by ingesting raw meat or insufficiently cooked meat as in roasted beef. As a result of this, an understanding of endoparasites in the wild (River Gudi) is essentially in order to find ways of avoiding zoonosis and excess loss if intensive aquaculture disease expected under intensive aquaculture.
Medical importance of fish parasite
In recent time, medically important parasite present in fishes have been source of concern to both medical practitioners and vertenarians. Parasitic infections are some of the factors hindering high fish productivity in fish farming [6]. In many parts of the world, there exists a wide body of knowledge on fish parasites and diseases as evidenced by enormous amount of literature and information available. Parasites are one of the most diverse and common pathogens the agriculturist may likely encounter as parasitic disease are very common all over the world and are of particular importance in the tropics [9]. The parasite of fish can either be internal or external. The parasitic infection of fish gives an indication of the quality of water as they generally increase the abundance and diversity in more polluted water irrespective of the species, either through injury to the tissue organs in the process of burrowing or consuming food or the removal of digested food in the gut of the fish as well as the secretion of proteolytic enzymes. C. gariepinus has been plagued by various parasites in the wild and cultured environment where they cause morbidity, mortality and economic losses in aquaculture practice in various parts of the world. Various helminth parasites have been incriminated in C. gariepinus infection such as adult Digenea infecting different tissues of the body; trematode cercaria of the family Clinostomidae encysting in tissues; and adult monogeneans of the families Pousopothocetylide, Dactylogyridae and Gyrodactylidae infecting the gills and skin. Trematodes are among the major parasites found affecting C. gariepinus, it damages the muscles of fish making it disgusting and unmarketable. In human flatworm causes a condition called Trematodosis. Fish roundworms (Nematodes) causes a condition in human called Aniskiasis. Fish tapeworms(cestodes) causes a condition in human called Diphyllobothriasis. C. gariepinus has shown high parasitemia of both medical and economic concern, it high level of endoparasites and ectoparasite may result in adverse conditions either to the aquatic system or to animals (human inclusive) who consumer this species of fish.
Reported parasite of Clarias Gariepinus across the geopolical zone of Nigeria
In Africa, a checklist of helminth parasites of freshwater fishes has been published by. and various reports also exist from different countries of Africa, highlighting on intensities, prevalence, epidemiology and pathology of such parasitic infections. According to, the Clarias harbor majority of the infections which include the adult Digenea infecting different tissues of the body; trematodemetacercaria of the family Clinostomidae encysting in tissues; and adult Monogenea of the families Pousopothocotylidae, Dactylogyridae and Gyrodactylidae infecting the gills and skin. However, another report by recorded that Clarias infections with adult trematodes were rare. According to him, the adults and larvae of cestodes, nematodes and acanthocephalans occur in the intestine. There is also an appreciable documentation of parasite fauna of Clarias gariepinus in Nigeria. One of the earliest reports inNigerian inland waters concerning fish parasites was that of [10] preliminary information on the parasites in the Kanji reservoir. They observed that not many fishes were infected. However, in a similar study by [11] in Maiduguri, Nigeria heavy parasitic infection of fish species was observed. Borno State has water bodies and most of the population is involved in fish production. So, with the information that parasites affect fish production, it is important to know the prevalence of these parasites [12]. Reported that Amonotaeria and Polyonchobothrium species of (cestodes; and Procamallanus species of nematodes and Neoechinorhynchus species of acanthocephalans in wild and culture Clarias gariepinus in Nigeria. mentioned that Caipillaria, contracaecum and cestodes in Clarias gariepinus caught from lake Hawassa, Ethiopia. As yet no epidemics of endoparasites have been reported in Nigeria, is likely that as fish culture becomes more intensive and widespread, fish parasites are likely to become a serious economic and health issues [6,13].
North west
At River Rima, Sokoto found Nematode (Procamallanus laeviconchus and Paracamallanus cyathopharynx), Cestode (Monobothrium wageneri) and Acanthocephalan (Neochinorhlynchus rutilli). In his investigation compare the presence of helminthic infections of some common species of fishes namely C. gariepenus and oreochromis niloticus in lake geriyo jimeta of Yola, Adamawa state where C. gariepinus, parasites were isolated Clinostomium species, Procammalanus species, Serradacnitis serrata and Wenyonia species the distribution of helminth parasites in the fishes showed a clear preference for the intestine as sites of attachment attributable to the availability of food in these regions. Observed a richer parasite species of hirudinae (Leech) and Achantogyrus spp in C. gariepinus from Lamingo Dam, Jos Nigeria. reported richer parasite species diversity (with much higher parasite prevalence of 40%) for both fish host species from Lake Geriyo in Yola, Adamawa state. They also reported Clinostomum spp. among the parasite found in both fish host types. Recorded the presence of tremades acantocephalan species and species of hurudinea in C. gariepinus from Sabon gari market of Zaria in Kaduna state [14].
North east
Encountered four parasitic species, these include, 2 protozoans Trichodina spp., Ichthyophthirius multifilis, and 2 Helminthes (cestodes) Diphyllobothrium dendriticum, Diphyllobothrium latum. Ichthyophthirus muftifilis in dam and pond samples examined in Bauchi metropolis. Sampled 100 species of C. garipinus from lake Alau in Maiduguri, Borno state. for endoparasite and ectoparasites, in which the following parasites where discovered. They include cestode, nematode and trematodes. The study shows that C. garipinus are afflicted by parasites that are of medical and economic importance. Project work in Tella Area of River Taraba by [15]. Revealed Macrogyrodactylus sp., monogeneans, Ergasilus sarsi, Tetracampos ciliotheca and Monobothrioides, woodland, which are cestodes and Procamallanus laevionchus, a nematode were recovered in the river [16].
South
Recorded the following from Ase River Catchment, Delta State; Trichodina, Epistylis spp, Chilodonella spp, Ichthyophthirius multifiliis, Camallanus polypteri, Procamallanus spiralis & Euclinostomum heterostomum. Iboh et al. (2016) both observed a richer parasite species of hirudinae (Leech) and Achantogyrus spp in C. gariepinus from Great kwara River in Cross River State. In Kwa River, Calabar, six helminths parasites recovered are Tapeworm species, Anisakis simplex, Nippostrongylus brasilienses, Ascaris lumbricoides, Caenorhabditis elegans and Ancyrocephalids monogeneans [17,18].
North central
In Abuja recorded Procamallanus laevionchus, Rhabdochona congolensis, Polyonchobothrium clariae, Allocreadium spp. & Heterophyidae spp. Parasites [19]. also recorded four species of helminthes parasites in Abuja comprises of two Cestodes, one nematode and one acanthocephalan isolated from the C. gariepius. The Cestodes were monobothrium sp and polyonchobothrium clariae. The nematodes were procamallanus laevionchus and the acanthocephalan was Neoechinorhynchus rutili. Equally found a low parasite species diversity (with only cestodes and nematodes) for C. gariepinus in Utako flowing gutter in Abuja, Nigeria [20]. Revealed Camallanus, Diphyllobothrium latum and Capillaria from River Gudi, Akwanga Local Government Area of Nasarawa State.
In where leeches (pisciola geometra) account for over 59% of the sample and midge larvae accounted for 41%. The rate of ectoparasites infestation of C. gariepinus in the University Research Fish Farm was observed to be high. Two kinds of ectoparasites (leech and midge larvae) were observed to be present on the skin of C. gariepinus. This might be because the skin is easily accessible by these parasites due to their direct contact with the surrounding water.
South west
Recorded presence of acanthocephalans in (Ibadan). In Osun State, Esa odo Reservoir, [21]. reported that trematodes (Clinostomum tilapiae), achantocephalans (Achantogyrus spp) and hirudinea (Leech) are the parasitic taxa recovered [22], recovered Procamallanus sp, Polyonchobothrium sp, Wenyonia sp, Pleurocercoid larva and Clinostomum sp from Ogun River and Asejire Dam in South-West. found Protozoa (Trypanosoma sp) in Lekki Lagoon, Lagos. Similarly, in Lekki Lagoon, Lagos, [23]. Recorded three cestodes Polyonchobothrium clarias, Stocksia pujehuni and Wenyonia acuminata and a nematode, Paracamallanus cyathopharynx.
South east
[24], carried out a survey on the endoparasites of C. garipinus in Owerri west local government area of Imo state. Where he reported the following endoparasite species of nematodes (Contracaecum and camallanus species), protozoans (cryptobia iubilans and trypanosoma species,) and acanthocephalans (acanthocephalus species). This result shows the presence and prevalence of endoparasite in owerri [25] In Abakaliki, recovered the following parasites Trichodina spp, Procamalanus spp & Heterobranchus spp (Table 1).
Conclusion
Clarias gariepinus examined for both endo and ecto parasites respectively in several work reviewed in here shows different parasites belonging to different groups. These include cestode, nematode, trematodes and Protozoan. This parasite is medically important to human and animals as it effect economic value of fish produced and raised public health concern in the different geopolitical zones in Nigeria [26-42].
uality assurance needs [14].
Acknowledgment
The authors of this review work wish to acknowledge Dr Adeniyi A.K. of Department of Biological Science, Federal University of Technology Minna, Niger State for his great support towards the success of this review paper
References
- Haruna AB (2006) Studies on the aspect of socio-economic factors influencing fish-farming in Adamawa State Nigeria. J Arid zone Fish 2(1): 8-14.
- Ashade OO, Osineye OM, Kumoye EA (2013) Isolation, identification and prevalence of parasites on Oreochromis niloticus from three selected River Systems. J Fish Aqua Sci 8: 115-121.
- Froese Ramer, Pauly Daniel (2014) Clarias gariepinus in Fish Base.
- Woo PT (2006) Fish Diseases and Disorders: Protozoan and Metazoan Infections, (2nd edn).
- Okoye Ikem C, Abu Simon J, Obiezue Ndunwanne NR, Ofoezie Ifeanyi E (2014) Prevalence and seasonality of parasites of fish in Agulu Lake, Southeast, Nigeria. Academic journals 13(3): 502-508.
- Imam TS, Dewu RA (2010) Survey of piscine ecto and intestinal parasites of Clarias sppsold at Galadima road fish market, Kano metropolis, Nigeria. Bioscience Research communications 22(4): 209- 214.
- Abdel Gaber R, El Garhy M, Morsy K (2015) Prevalence and Intensity of Helminth Parasites of African Catfish Clarias gariepinus in Lake Manzala, Egypt. Advances in Bioscience and Biotechnology 6: 464-469.
- Angera SM (2008) Endo parasites of selected freshwater fish species Clarias gariepinus, Heterobranchus longifilis and Oreochromis niloticus in lower Benue valley. project work. University of Agriculture Markurdi. Anguillaris from Bida Floodplain of Nigeria. Journal of Applied Sciences and Environmental Management pp. 839-844.
- Akinsanya B, Otubanjo OA (2006) Helminth parasites of Clarias gariepinus (clariidae) in Lekki lagoon, Lagos, Nigeria. Revista de Biologia Tropical 54(1): 93-99.
- Oluorin KB, Somorin CA (2006) Intestinal helminths of fish of Owa stream South-West Nigeria. Res J Fish Hydrobiol 1(1): 6-9.
- Allumma MI, Idowu RI. (2011) Prevalence of gill helminths of Clarias gariepinus in Baga side of Lake Chad. J Appl Sci Environ Manage 15(1): 47-50
- Ayanda OI (2009) Comparative parasitic helminths infection between cultured and wild species of Clarias gariepinus in Ilorin, North Central Nigeria. Scientific Research and Essay 4(1): 18-21.
- Adam AM, Murrell KD, Cross JH (1997) Parasites of fish and risks to Public Health. Rev Sci Tech 16(2): 652-660.
- Magami, Ibrahim Muhammad, Enodiana, Ignatus Osamiabe, Ladan, et al. (2016) Prevalence of Gastrointestinal Helminthes in Clarias gariepinus and its Fishing Practices at River Rima, Sokoto Nigeria. International Journal of Pure and Applied Bioscience.
- Udechukwu Chukwunonso Uche, Panda Sam Mao, Sunday Inusa Danladi, Bello Fatima Adeola (2018) Parasites associated with Clarias gariepinus (African catfish) from dam, plastic and concrete ponds in Bauchi metropolis, Bauchi State, Nigeria.
- Mathias Simon Bingari (2014) Gill Digestive Tract Parasites of Clarias Species in the Tella Area of River Taraba, Taraba State, Nigeria.
- Edore Edwin Ito (2017) Tropical Disease Research Unit, Department of Animal and Environmental Biology, Delta State University, P.M.B 1, Abraka, Nigeria Survey of parasites of two fish species (Tilapia zillii and Clarias gariepinus) in Ase River Catchment, Delta State, Nigeria. Journal of Coastal Life Medicine.
- Cletus Inah Iboh, Raymond Odey Ajang (2016) Helminths Parasitic Infection of Clarias Gariepinus from Great Kwa River, Cross River State, Nigeria. European Journal of Pharmaceutical and Medical Research ejpmr 3(12): 101-105.
- SM Kawe, RO God spower, MR Balarabe, RI Akaniru (2016) Prevalence of gastrointestinal helminth parasites of Clarias gariepinus in Abuja, Nigeria. Sokoto Journal of Veterinary Sciences 14(2): 26-33.
- Aliyu MD, Solomon JR (2012) The Intestinal Parasite of Clarias Gariepinus Found at Lower Usman Dam, Abuja. Researcher 4(9): 38- 44.
- Absalom KV, Makpo JK, Mustapha AJ (2018) Prevalence of Gastrointestinal Helminth Parasites of Clarias gariepinus at River Gudi, Akwanga L.G.A. of Nasarawa State, Nigeria. International Journal of Fisheries and Aquaculture Research 4(1): 9-15.
- Olugbotemi Caleb Ibironke, Olajumoke Abimbola Morenikeji, (2018) Helminth Parasites of Clarias gariepinus (Burchell, 1822) and Oreochromis niloticus (Linnaeus, 1758) from Esa Odo Reservoir, Esa Odo, South-West Nigeria 10(8).
- Salawu MT, Morenikeji OA, Sowunmi AA, Odaibo AB (2012) Comparative survey of helminth parasites of Clarias gariepinus (Burchell, 1822) and (Boulenger, 1903) from the Ogun River and Asejire Dam in south-west Nigeria Clarias pachynema. International Journal of Fisheries and Aquaculture 5(1): 7-11.
- Akinsanya B, OA Otubanjo (2005) Helminth Parasites of Clarias gariepinus (Clariidae) in Lekki Lagoon, Lagos, Nigeria.
- Okoye Uzodinma O, Ndupuh EE, Adeleye SA (2016) A survey on endoparasites of Clarias gariepinus in some selected fish farms in Owerri west local government area of Imo State, Nigeria. International Journal of Fisheries and Aquatic Studies 4(5): 624-631.
- Ogonna C Ani, Emmanuel I Nnamonu, Cynthia Ejiogu (2017) Prevalence of Intestinal Parasites of Fish Farmed and Harvested in Abakiliki, Nigeria: A Pointer to the Level of their Vulnerability. International Journal of Research in Pharmacy and Biosciences 4(9): 7-10.
- Abdel Gaber R, Garhy Mel, Morsy K (2011) Prevalence and intensity of Helminth Parasites of African Lake Chad. J Appl Sci Environ Manage 15(1): 47-50.
- Abdel-Gaber R, Abdel-Ghaffar F, Bashtar AR, Morsy K, Saleh R (2016) Interactions between the intestinal cestode Polyonchobothrium clarias (Pseudophyllidea: Ptychobothriidae) from the African Sharp tooth catfish Clarias gariepinus and heavy metal pollutants in an aquatic environment in Egypt. Journal of Helminthology 90(6): 742-752.
- Adegoroye F, Omobhude M, Morenikeji O (2019) Helminth Parasites of Synodontis clarias (Linnaeus, 1758), Chrysichthys nigrodigitatus (Lacepede, 1802) Chrysichthys auratus (Geoffrey Saint-Hilaire, 1808) in Asejire Dam, South-West Nigeria. International Journal of Aquatic Science.
- Bednarska M, Besdnarski M, Soltysiak Z, Polechonski R (2009) Invasion of Lernaea cyprinacea in Rainbow Trout (Oncorynchus mykiss). ACTA Scientiarum polonorum medicina Veterinaria 8(4): 27-32.
- Bhuiyan AS, Musa ASM (2008) Seasonal prevalence and intensity of infestation by ectoparasites in Carps relating to phyico-chemical parameters in some ponds of mymensingh and Bogra districts of Bangladesh. Banglash journal of scientific and Industrial Research 43(3): 411-418.
- Bichi AH, Bawaki SS (2010) A survey of ectoparasites on the Gills, skin and fins of Oreochromis niloticus at Bagauda fish farm, Kano, Nigeria. Bayero Journal of Pure and Applied Science 3(1): 83-86.
- Bush AO, Fernandez JC, Esch GW, Seed R (2001) Parasitism: The diversity and ecology of animal parasites. Cup, Cambridge, UK.
- Dankishiya AS, Oboh A, Ibrahim UB (2013) The prevalence of Helminth parasites in the gastro- intestinal tract of wild African sharptooth catfish Clarias gariepinus (Siluriformes: Clariidae) in Gwagwalada, Nigeria. Research Journal of the Costa Rican Distance Education University 5(1): 83-87.
- Echi PC, Eyo JE, Okafor, FC (2009) Co-infection and morphometrics of Three Clinostomatids Digenea: Clinostomatids. In: Tilapia guinensis Bleeker,1862 from Opi lake, Nigeria. Bio Research 7(1): 432-436.
- Hassan AA, Akinsanya Bamidele, Adegbaju WA (2007) Haemoparasites of Clarias Gariepinus and Synodontis Clarias From Lekki Lagoon, Lagos Nigeria. Journal of American Science 3(3).
- Hussein A, Tefera M, Asrate S (2012) Gastrointestinal helminths parasites of Clarias gariepinus (catfish) in Lake Hawasa, Ethopia. Scientific Journal of Animal Science 1(4): 131-136.
- Khalil LF, L Polling (1997) Checklist of the helminth parasites of African freshwater fishes. University of the North Republic of South Africa.
- KV Absalom, JK Makpo AJ Mustapha (2018) Prevalence of Gastrointestinal Helminth Parasites of Clarias Gariepinus at River Gudi, Akwanga Local Government Area of Nasarawa State, Nigeria. International Journal of Fisheries and Aquaculture Research 4(1): 9-15.
- Skelton P, Teugels GG (1992) Neotype description for the African catfish Clarias gariepinus (Burchell, 1882) (Pisces: Siluroidei: Clariidae). Ichthyol. Bull 56: 1-7.
- Woo PTK (1987) Cryptobia and cryptobiosis in fishes. Adv Parasitol 26: 199-237.