Extracción de compuestos fenólicos

The role of biotic factors in shaping parasite distributions are well documented and include differences between the host sexes (Poulin 1996, Klein 2000, Arneberg 2002, Zuk 2009) and host age classes (Anderson and Gordon 1982, Anderson and Medley 1985, Pacala and Dobson 1988, Grenfell et al. 1995, Anderson and May 1991) but there is less literature on the role of additional biotic factors such as diet and biodiversity within the habitat of the parasite. Recently however, Thieltges et al. (2008) review the significant impact of biotic factors including biodiversity on parasite transmission success. Below, a number of key interacting biotic factors that are associated with trematode population dynamics in the definitive host are, briefly, outlined.

2.4.1 Diet

For diseases that are trophically transmitted, host diet ultimately defines whether or not an individual will become infected, and differences in parasite loads can be explained therefore by host prey choice. Clonorchis sinensis cases in China are more prevalent in men compared to women because males consume more raw fish (Lun et al. 2005). Host diet can have additional repercussions for parasite fecundity (Molan and James 1984), such that the fitness of a parasite increases with the resources available within the host habitat. This is confounded, however, by the increased host resistance that parallels the nutritional status of the host (Bize et al. 2008) and consequently, the success of the parasite is a compromise between these two components (Bize et al. 2008, Heylen and Matthysen 2011). Further, starving parasites at earlier life stages can have repercussions for the success, fecundity and longevity of the parasites once in the definitive host (Davies et al. 2001, Walker et al. 2006). Both the susceptibility of the host, and also the fecundity of the parasite can be impacted therefore by host diet.

2.4.2 Host sex and age

Sex biased parasitism has been reported extensively in the literature (Poulin 1996, Klein 2000, Arneberg 2002). In mammals there is a general trend for males to suffer greater prevalence, intensity of infections and severity of disease (Klein 2004, Zuk 2009), with consequent repercussions for host reproduction depending on mating system and parasite

LITERATURE REVIEW

19 virulence (see Moore and Wilson 2002, Miller et al. 2007). These sex differences have been related to hormonal differences (Klein 2000), behavioural disparities including home range size (Bundy 1988) and dispersal strategies (Greenward 1980), aggressiveness (Restif and Amos 2010) and foraging strategy (Anderson et al. 2004). All these can affect an individual’s ability to compete for resources or a mate and, ultimately result in contrasting risks of infection, disease establishment and / or severity (Lindsey and Altizer 2009). In mammals, polygynous mating systems create morphological and physiological differences between males and females because of competition for mates (Zuk 2009). The resulting male-biased dimorphism (where one sex is larger than the other), on the simplest level, means males become a larger target for parasites (Poulin 1996, Arneberg 2002, Moore and Wilson 2002). There is some evidence that larger parasites carry more eggs (Poulin 1996, Hanelt 2009) and that larger hosts have larger parasites (Loot et al.

2011), so in mammalian systems, males are hypothesised to carry more, and larger, parasites (Poulin 1996) but availability of such data is rare. In addition, an increased body mass is linked to decreased leucocyte counts (Semple et al. 2002) causing the larger sex to suffer from increased pathology. Such variation in response to disease appears to result in differences in parasite infra-population size (Klein 2000), transmission rate (Perkins et al. 2003, Ferrari et al. 2004), and the genetic structure of the parasitic population (Caillaud et al. 2006). Recently it has been shown that male mammalian hosts may also shed more infective particles (for example, eggs) than their female conspecifics (Lin et al.

2006). Yet F. hepatica, which lacks prevalence differences between the host sexes (Mas-Coma et al. 1999), is most fecund within female hosts (children Homo sapiens in Peru) such that females produced c. 400 eggs per gram (epg) whilst parasites in male hosts produced only c. 100 epg (Esteban et al. 2002).

The prevalence of infections in mammals from the UK tended to show no difference between the sexes (Table 2.2) perhaps because diet is similar among the sexes for most mammals. Additional space and resources for parasites within the host habitat in the larger males, alongside a greater consumption of potentially infected fish, could explain infection intensity differences between male and female hosts where apparent (see Table 2.2; Frankland 1959). Predominantly male biases were observed in trematode infections of definitive hosts for studies outside the UK (see Klein 2004) so perhaps habitat and weather related factors cause increased differences between male and female behaviours elsewhere resulting in increased exposure to helminths of males but this geographic difference requires further study.

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20 Table 2.2 Trematodes of Mammals in England, Wales and the Isle of Man recorded on the Natural History Museum Host-Parasite Database (as of August 2012, excludes Zoo animals); The directional effects of host sex, host age and host health on trematode prevalence P, abundance A, intensity I or fecundity F within the definitive mammalian host is presented where available in the literature. *Data additionally incorporated by the authors. NUK = Relationship identified in a study on a non-UK mammal. NS = No significant difference reported).

Parasite Mammalian Host Effect

Class Species Host Sex Host Age Host health

Brachylaemidae B. recurva Apodemus flavicollis¹ A. sylvaticus²

Rattus norvegicus¹

Vulpes vulpes³ NS³ NS³

Ityogonimus lorum Meles meles¹

Talpa europaea⁴ NS²¹

I. talpae Talpa europaea⁴

Dicrocoeliidae Corrigia vitta Apodemus flavicollis¹ A. sylvaticus²

Arvicola terrestris¹ Clethrionomys glareolus¹ Microtus agrestis¹

NS²² Increased P with age^2,22

Dicrocoelium dendriticum

Myocastor coypus¹

Ruminants²⁰ P higher in females²³ Increased P and I with age²³ F increases if host stressed²⁴

Fasciolidae Fasciola hepatica Bos taurus⁵ Compromised health

with respect to additional infection²⁵

Heterophyidae Cryptocotyle lingua Vulpes vulpes³ NS³ NS³

Microphallidae Microphallus pygmaeus

Mus musculus¹⁸ I higher in males²⁶ F higher in older conspecifics but NS²⁶ Omphalometridae Omphalometra

flexuosa

Talpa europaea⁴ NS¹³

Opisthorchiidae Clonorchis sinensis Homo sapiens¹⁹ P higher in males²⁷

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21 References to Table 2.2

1Harris, S., Yalden, D.W. (eds.) (2008) Mammals of the British Isles: handbook (4^th Edition). Blackwell Scientific Publications. Southampton pp. 799.

2Behnke, J.M., Lewis, J.W., Zain, S.N.M., Gilbert, F.S. (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73: 31-44.

3Richards, D.T., Harris, S., Lewis, J.W. (1995) Epidemiologic studies on intestinal helminth-parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Veterinary Parasitology 59: 39-51.

4Davies, E. (1932) On a trematode, Ityogonimus lorum (Duj, 1845), with notes on the occurrence of other trematode parasites of Tapla europaea in the Aber-ystwyth area. Parasitology 24: 253-259.

5Hughes, D.L., Purnell, R.E., Brocklesby, D.W. (1977) The effect of initial Fasciola hepatica infection on the pathogenicity of subsequent Babesia divergens infections in intact and splenectomised calves. Veterinary Record 100: 320-321.

18Brayton, A.R., Brain, P.F. (1974) Effects of crowding on endocrine function and retention of digenean parasite Microphallus pygmaeus in male and female albino mice. Journal of Helminthology 48: 99-106.

Metorchis albidus* Lutra lutra NS* I higher in adults* Males show greater

pathology*

Pseudamphistomum truncatum*

Lutra lutra Mustela vison

NS* I higher in adults* Males show greater

pathology*

Schistosomatidae Schistosoma haematobium

Homo sapiens⁷ (NUK) NS in P²⁸ (NUK) P increases with age until c.15 years²⁸, but

S. japonicum Mus muculus⁶ Associated with

biochemical changes

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22

19Dennis, M.J.S., Dennison, A.R., Morris, D.L. (1989) Parasitic causes of obstructive jaundice. Annals of Tropical Medicine and Parasitology Liverpool 83:

159-161.

6Littlewood, D.T.J., Johnston, D.A. (1995) Molecular phylogenetics of four Schistosoma species determined with partial 28S ribosomal RNA gene sequences.

Parasitology 111: 167-175.

7Wiselka, M.J., Nicholson, K.G. (1993) Schistosomiasis in Leicester. Journal of Infection 26: 177-179.

9Walker, T.K., Simpson, A.J.G., Rollinson, D. (1989) Differentiation of Schistosoma mansoni from S. rodhaini using cloned DNA probes. Parasitology 98:

75-80.

10Imbert-Establet, D., Mone, H., Coulson, P.S., Wilson, R.A. (1998) Schistosome-induced portacaval haemodynamic changes in Rattus rattus are associated with translocation of adult worms in lungs. Parasitology 116: 237-241.

20Otranto, D., Traversa, D. (2003) Dicrocoeliosis of ruminants: a little known fluke disease. Trends in Parasitology 19: 12-15.

21Ribas, A., Casanova, J.C. (2005) Helminths of Talpa europaea (Insectivora, Talpidae) in southwestern Europe. Acta Parasitologica 50: 161-167.

22Abu-Madi, M.A., Behnke, J.M., Lewis, J.W., Gilbert, F.S. (2000) Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74: 7-15.

23Ducommun, D., Pfister, K. (1991) Prevalence and distribution of Dicrocoelium dendriticum and Fasciola hepatica infections in cattle in Switzerland.

Parasitology Research 77: 364-366.

24Sotiraki, S.T., Leontides, L.S., Himonas, C.A. (1999) The effect of transportation and confinement stress on egg production by Dicrocoelium dendriticum in sheep. Journal of Helminthology 73: 337-339.

25Mas-Coma, S., Bargues, M.D., Esteban, J.G. (1999) Human fasciolisis. In: Fasciolosis (ed.) Dalton, J.P. CAB International Publishing, Wallingford, Oxon, UK, pp. 411-434.

26Molan, A.L., James, B.L. (1984) The effects of sex, age and diet of mice and gerbils on susceptibility to Microphallus pygmaeus (Digenea: Microphallidae).

International Journal for Parasitology 14: 521-526.

13Frankland, H.M.T. (1959) The incidence and distribution in Britain of the trematodes of Talpa europaea. Parasitology 49: 132-142.

27Lun, Z-R., Gasser, R.B., Lai, D-H., Li, A-X., Zhu, X-Q., Yu, X-B., Fang, Y-Y. (2005) Clonorchiasis: a key foodborne zoonosis in China. The Lancet Infectious Diseases 5: 31-41.

28Tchuem Tchuente, L-A., Behnke, J.M., Gilbert, F.S., Southgate, V.R., Vercruysse, J. (2003) Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8: 975-986.

29Shaw, D.J., Vercruysse, J., Picquet, M., Sambou, B., Ly, A. (1999) The effect of different treatment regimens on the epidemiology of seasonally transmitted Schistosoma haematobium infections in four villages in the Senegal River Basin, Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 93: 142-150.

30 Weil, C., Kvale, K.M. (1985) Current Research on Geographical Aspects of Schistosomiasis. Geographical Review 75: 186-216.

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23 In addition to host sex differences, parasite prevalence and intensity can be typically and positively associated with host age through the cumulative risk of exposure with time (Anderson and Gordon 1982, Anderson and Medley 1985, Pacala and Dobson 1988, Grenfell et al. 1995, Anderson and May 1991). Essentially, where parasites across the host population become less aggregated with host age, then density-dependent effects such as acquired immunity are acting on the parasite population (see Quinnell et al.

1995). Trophically transmitted parasites tend to accumulate with host age but parasite fecundity decreases as the parasite ages (see Table 2.2; Shaw et al. 1999). This has implications for disease spread because hosts that have been infected for a longer period may have more parasites but release less infective units (eggs) than younger conspecifics carrying fewer parasites. If the host continuously acquires more parasites, however, the overall fecundity of the individual hosts’ parasite population (and release of eggs into the environment) will remain high. Further, host resistance against parasites is heritable resulting in generational differences in parasite load and / or fecundity across the host population (Smith et al. 1999).

2.4.3 Parasite competition and co-infection

Trematode populations may be regulated further through density-dependent mechanisms such as competition (Madhavi et al. 1998). Both intra- and inter- specific competition can impact the life history strategy (Jackson et al. 2006, Lagrue and Poulin 2008) and transmission success (Pederson and Fenton 2007) of co-habiting species. For example, a higher proportion of Coitocaecum parvum exhibited progenesis when the molluscan host was co-infected with Microphallus sp. (see Lagrue and Poulin 2008). Competitive exclusion within the snail intermediate host limits the number of multiple helminth infections (Soldanova et al. 2012). In addition, pre exposure can limit the intensity of trematode infection where the host immune system is primed and this acquired immunity can protect the host from secondary species infection (Luong et al. 2011). Processes such as intraspecific competition are perhaps less important for trematodes because a large proportion of early life-stage parasites (for example, cercariae) die prior to transmission which results in naturally low recruitment rates (see Underwood 1979, Keough and Chernoff 1987).

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24 The likelihood of co-infection can change depending on the life-stage of the parasite species. Trematodes have different requirements at different life stages: trematodes reproduce in the first intermediate and definitive hosts, whilst the second intermediate host (fish) can be viewed as a transmission vehicle. The resulting intensity of competition between parasites at each life stage will therefore differ considerably (Karvonen et al.

2012 but see Niewiadomska and Pojmańska 2011). Karvonen et al. (2012)’s recent hypothesis suggests that co-infections will be less common in snails than in fish because resources in the snail are limited so that trematodes would be negatively affected at this life stage. Conversely, resources are not limited in the fish when the parasite is dormant.

In addition, there is a benefit to co-infection from the parasite’s perspective because species specific responses to cysts by the host are less likely to develop as a consequence of continual exposure to generic species. This hypothesis was supported by observed low levels of co-infection in snails and high levels in fish (Karvonen et al. 2012).

Alternatively, such a trend may result from sheer numbers: in snails, a single parasitic unit (sporocyst) produces thousands of clones (cercariae) perhaps restricting space for further trematode infections so that the first parasite to infect a snail becomes dominant.

Conversely, the low impact metacercariae, encysting on fish, have little impact on the space or resources of the fish host. Under natural conditions, co-infections are common and considered the norm (for example Lello et al. 2004, Pederson and Fenton 2007, Telfer et al. 2010). In mice, co-infection with multiple strains of Trypanosoma brucei mitigated the negative pathological effects caused by single strain infections (Balmer et al. 2009) and perhaps this acts to alleviate the major effects of infections in natural populations.

The parasite genotype may interact with the number or type of parasites infecting a single host to influence the overall distribution and assembly of parasites. For example, the probability of multiple infections of Microbotryum violaceum apparently depends on the genotypes of the particular interacting strains (Koskella et al. 2006). In the dioecious schistosomes, genetic structure differs between the sexes (see Prugnolle et al. 2003) with c. 50% of genes biased to a particular sex (Beltran and Boissier 2010). Schistosomes are monogamous and demonstrate male biased sex ratios in wild populations (Beltran et al.

2009), although this ratio can be altered by ecological variables (see Mone 1997). As a

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