Long-term dynamics ofLigula intestinalisand roachRutilus rutilus: a study of three epizootic cycles over thirty-one years

Abstract

Data are presented on 2 full epizootic cycles and the start of a third of Ligula intestinalis in roach Rutilus rutilus in a small lake, and the relationships of these cycles to the densities of rudd, Scardinius erythrophthalmus, and Great Crested Grebes, Podiceps cristatus, over 31 years. The parasite was introduced to the lake by P. cristatus in 1973 at a time when the roach population had increased in response to eutrophication to a level at which individual fish growth was stunted and the hithero dominant rudd population had declined in numbers as a consequence of inter-specific competition with roach. Ligula prevalence peaked at 28% in only 2 years: thereafter parasite-induced host mortality caused a decline in the roach population, releasing fish from stunting and allowing the rudd population to recover. The consequent improved growth of roach individuals and their short life-span reduced Ligula transmission rates and prevalence levels declined to approximately 1% although Ligula nevertheless persisted for a further 10 years. Following a massive winter-kill of the fish populations in 1984-1985, fish and Ligula numbers declined to barely detectable levels and the parasite disappeared from samples. Rudd recovered first, then roach and interspecific competition again led to a decline in rudd numbers. This increase in roach numbers led to a decrease in roach growth rates, which coincided with the re-colonization of the lake by Ligula. This second epizootic of Ligula peaked within 2 years in 1991-1992, when up to 78% of roach were infected with a maximum abundance of 2.2 parasites and intensity of 21 parasites. Heavy parasite-induced mortality of roach led to a decline in numbers, an improvement in individual growth rate and a reduction of Ligula transmission rates such that the epizootic died out in 1996. Similar conditions of roach numbers and growth prevailed at the start of a third cycle in 1998. The course of events over the second cycle was so similar to that of the first that it confirms the interpretations of that cycle. Comparison with other localities shows that epizootics of Ligula always coincide with rapid increases in roach numbers, for whatever cause, and stunted growth, which together attract piscivorous birds. At the start of a cycle Ligula is a major determinant of the population dynamics of the roach, but at the end of the cycle the fish population dynamics determine those of the parasite. The cycles are not regulated and the roach-Ligula system is inherently unstable.

The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus

“…As has been noted previously by Kennedy et al (2001) and Loot et al (2001Loot et al ( , 2002, our data suggest that Ligula may have a small inhibitory effect on body length, weight and condition in young fish (i.e. 2 years old).…”

“…steroid receptors), which are necessary for the process of gametogenesis, may be disrupted, thus preventing brain activation and subsequent initiation of puberty. Furthermore, peripheral stimulators and inhibitors, active at all levels of the brain-pituitary-gonadal (BPG) axis, may be targets of the putative hormonal disruption by Ligula, which results in an inability of the gonads to respond to hormonal signals.As has been noted previously by Kennedy et al (2001) and Loot et al (2001Loot et al ( , 2002, our data suggest that Ligula may have a small inhibitory effect on body length, weight and condition in young fish (i.e. 2 years old).…”

The occurence and dynamics of Ligula intestinalis in its cyprinid fish host, tench, Tinca tinca in Mogan Lake (Ankara, Turkey)

“…According to Kennedy et al (2001), Ligula typically exhibits epizootic cycles over a period of 4-5 years and it has excellent powers of dispersal and is brought into a lake by migratory birds. Following its arrival in a lake, if the conditions are suitable, its population increases rapidly which in turn results in mortality of fish hosts because of parasite-induced host mortality (PIHM) (Loot et al, 2001a).…”

“…Following its arrival in a lake, if the conditions are suitable, its population increases rapidly which in turn results in mortality of fish hosts because of parasite-induced host mortality (PIHM) (Loot et al, 2001a). Since the whole fish population may be infected in the course of time (Kennedy et al, 2001), there would be a decrease in the fish population because of PIHM. This will also decrease the Ligula population because of not being able to complete its life cycle.…”

Ecosystem services provided by waterbirds

“…For example, terns are final hosts for trematode parasites that use mosquitoes as intermediate hosts (Fonteneau et al, 2009). Cestodes that use piscivorous birds as final hosts can reduce the abundance of introduced cyprinids (Kennedy, Shears & Shears, 2001). Since the life cycle of most helminth parasites remains unknown (Lefebvre et al, 2009) (see also https://web2.uconn.edu/tapeworm/index.php), birds are likely to carry many more parasites of pests than is currently known.…”