4.0 DISCUSSION
L. intestinalis has a strong negative effect on the fecundity of
its intermediate host, E. sardella . Such an effect, which was
also found in other fish host species, thus seems widespread throughout
the species range of this parasite (Barson and Marshall, 2003; Carter et
al., 2005; Cowx et al., 2008). We also found that the relative weight of
gonads in relation to body size increased over the 10-year duration of
this study, and observed a decline in somatic growth at maturity (from
stage IV to stage V). These temporal changes were found in non-infected
fish, which indicates that they may reflect evolutionary changes in the
life history of E. sardella .
Organisms are selected for changes in life history traits when
age-specific death or fecundity rates are changed (Forbes, 1993). In our
study, we observed an overall 69% lower fecundity in infectedversus uninfected hosts, that is, the cestode L.
intestinalis caused a significant partial castration in E.
sardella . Reduced host fecundity is a common outcome associated with
parasite infection (Hurd, 2001) and contribute to reduced host fitness
(Gooderham and Schulte-Hostedde, 2011). Infected hosts may compensate
for this fitness loss by shifting their life histories towards earlier
reproduction (Jokela and Lively, 1995; Lafferty, 1993b). Many host
species have been shown to increase their early reproductive output if
their chances for future reproduction are reduced (Adamo, 1999;
Minchella and Loverde, 1981).
Our observations of an increase in gonadal weight in relation to fish
body size suggest that reproductive investment in E. sardella has
increased at the expense of investment in somatic growth after reaching
maturity. These findings are consistent with our prediction that their
life histories should shift towards earlier reproduction. The fact that
they come from an analysis of the non-infected fish indicates that this
change is not a secondary effect of infection. More work is warranted,
however, to determine whether it is caused by plastic or evolutionary
responses.
A parasitic relationship between L. intestinalis and E.
sardella in Lake Nyasa was first observed in 1996 (Mwambungu et al.,
1996). An earlier study investigating the breeding biology and in
particular examining the ovaries of E. sardella between 1992 and
1994, did not report any case of L. intestinalis infection
(Thompson, 1996). We believe this suggests that this tapeworm was likely
absent from Lake Nyasa prior to the late 1990s. After the first
observation, E. sardella in the lake kept being found infected byL. intestinalis , as manifested by the work of J.K.Kihedu (MSc
thesis, Sokoine University of Agriculture, Tanzania, 2006, unpublished
data). The earliest sampling year in our study is 2005, where prevalence
is estimated at 50%. This indicates that L. intestinalis has
spread steadily, and therefore that selection caused by this parasite on
its host has increased during the early years after introduction.
A shift towards investment in current reproduction has been reported in
many other host-parasite systems, where infected hosts increased their
reproductive effort before dying or being castrated by the parasite. In
insects, Polak and Starmer (1998) observed that experimentally
parasitized male Drosophila nigrospiracula infected with a mite
(Macrocheles subbadius ) lived shorter lives, but before dying
they courted females significantly more than non-parasitized controls.
Further, Adamo (1999) observed that female crickets (Acheta
domesticus ) increased egg laying in response to infection with the
bacterium Serratia marcescens . In snails, Minchella and Loverde
(1981) and Thornhill et al. (1986) observed an increase in reproductive
output in female Biophalaria glabrata parasitized by a castrating
trematode Schistosoma mansoni . In crustaceans, Chadwick and
Little (2005) observed that Daphnia magna infected with a
microsporidian Glugoides intestinalis shifted their life-history
towards early reproduction. In birds, Sanz et al. (2001) observed that
female pied flycatchers (Ficedula hypoleuca ) with hemoparasite
infection initiated egg laying earlier and laid larger clutches. In
reptiles, Sorci et al. (1996) observed that common lizards
(Lacerta vivipara ) increased their reproductive investment after
being infected with haematozoans. More examples where reproduction is
seen to increase with the onset of infection have been reviewed in
Schwanz (2008). Taken together, these studies show that parasites, by
affecting the future reproductive success of their hosts, induce life
history changes in infected hosts, and that these plastic changes are
adaptive.
Here we observe a shift towards increased reproductive effort at the
expense of somatic growth across generations, in non-infected hosts.
This pattern, which cannot be explained by plastic life history
responses to infection, might reflect adaptation to recent selective
changes in Lake Nyasa. Importantly, increased parasite pressure may not
be the only environmental change that has taken place in Lake Nyasa over
the last couple of decades. Other potential sources of selection for
earlier reproduction include: fishing (Fenberg and Roy, 2008; Heino and
Godø, 2002; Hutchings and Fraser, 2008; Jorgensen et al., 2007;
Jørgensen et al., 2009; Kuparinen and Merilä, 2007; Sharpe and Hendry,
2009; Sharpe et al., 2012); increased predation by native or introduced
species (Hampton et al., 2018; Sharpe et al., 2012); and fluctuations in
zooplankton abundance that may induce earlier maturation.
Most evidence of fishery-induced evolution comes from large, heavily
exploited fish population stocks (e.g. North Arctic cod) where
industrial fishing using trawlers has been in practice for many years.
On the contrary, the Lake Nyasa E. sardella fishery is mainly
traditional, operating in near-shore lake zones using paddled dugout
canoe crafts (Mwambungu and Ngatunga, 2001). Over the past decades,
however, fishing effort catch rates have decreased in Wissman Bay, where
the present study was conducted. (Figure S1).
Increased fishing effort has also been reported for other fish species
than E. sardella in riparian countries around lake Nyasa such as
Tanzania (Irvine et al., 2018; Irvine et al., 2002), Mozambique (Halafo
et al., 2004; Irvine et al., 2018) and Malawi (Irvine et al., 2018; Weyl
et al., 2010).
In the present study, E. sardella were sampled using the
traditional fishing method. The majority of the sampled fish was
composed of individuals of the body sizes between 50-100 mm in length
(Figure S2), which corresponds to mature fish (i.e. from stage IV
and above). This suggests that the traditional E. sardellafishing practice is probably size-selective and induces a higher
mortality in adults than younger fish. Interestingly, the number of
tones landed per fisherman (which can be considered as representing
stock density) dramatically decreased in 2013 (Figure S1), following
three consecutive years with both high L. intestinalis prevalence
(strongly reducing E. sardella fecundity) and sustained fishing
effort (increased adult mortality) (Figure S1). Therefore, we argue that
parasitism by L. intestinalis may have acted synergistically with
fishery-mediated selection in driving what appears like an evolutionary
shift towards earlier life history of E. sardella in Lake Nyasa.
Increased predation by native or introduced organisms could also be one
factor affecting selection on life history traits of E. sardella .
In the native cyprinid fish Rastrineobola argentea in Napoleon
Gulf of Lake Victoria, Sharpe et al. (2012) observed decreased body
size, maturation at smaller sizes and increased reproductive effort in
response to the introduced predator fish Lates niloticus .
However, in contrast to Lake Victoria and many other ancients lakes
where dozens of non-native species have been introduced over the past
decade (Hampton et al., 2018), in Lake Nyasa no new introduced predator
for E. sardella has been reported so far. The primary natural
piscivorours predators of E. sardella in this lake are the
pelagic haplochromine cichlids from the genera Ramphochromis,
Diplotaxodon, and Copadichromis, as well as the larger cyprinidsOpsaridium microlepis and O. microcephalum . Increased
abundance of the native predators of E. sardella over time in the
lake could have selected for life history changes similar to those
observed here. Unfortunately, the area where the present study was
conducted is a data-poor region; the last pelagic ecosystem stock
assessment was conducted between 1991-1994 (Menz (1995). Recent time
series on the abundance fluctuations of the natural predators ofE. sardella are lacking. Further research, particularly on the
combined effects of parasitism, fishing, and natural predation onE. sardella in Lake Nyasa, would be highly valuable, given the
ecological and economical importance of this fish species.
Another factor that could have affected selection on the life history
traits of E. sardella in Lake Nyasa may be concomitant increases
in the prevalence of other parasites. In their naturally habitats hosts
are usually infected by two or more different parasite species (Kotob et
al., 2017; Petney and Andrews, 1998). To the best of our knowledge, the
only other parasite that has been reported to infect E. sardellais the nematode Camallanus sp. (Mgwede and Msiska, 2018). In the
present study, we caught 3,488 wild, i.e. naturally-infectedE. sardella , none of them observed with Camallanus sp.
infection.
Overall, this study reveals that life history of E. sardella in
Lake Nyasa has been shifting, over a period corresponding to the
invasion of this lake by a castrating parasite. It remains correlative,
and more work is needed to examine the evolutionary nature of these
changes. Yet the cestode L. intestinalis , by strongly reducing
the fecundity of its host, appears as likely as fisheries to drive such
evolution. Our study suggests that these two types of selective factors
may have acted in synergy.