1.0 INTRODUCTION
Life history theory assumes that there are trade-offs between different
traits in organisms, such as growth, reproduction and survival (Roff,
2002). These traits cannot be simultaneously maximized within the same
individual because the available amount of nutrients and other resources
are in limited supply (Stearns, 1989). Increased resource allocation
into one trait will, therefore, come at the cost of reduced allocation
into other traits (Agnew et al. , 2000). In each given
environment, the optimal way to resolve these trade-offs (i.e.,the optimal strategy for maximizing fitness) is the one achieving the
highest possible reproductive success (Pianka, 1976; Stearns, 1989;
Agnew et al. , 2000). For instance, if adult mortality increases
within a population (e.g., due to increased predation),
individuals that mature relatively earlier and invest relatively more
into current reproduction versus future survival will be favoured
by natural selection (Fredensborg and Poulin, 2006).
For fish, both natural predation and fishing (i.e., predation by
humans) are important selective factors that drive adaptive changes in
life history traits such as developmental rates and timing of
reproduction (Heino and Godø, 2002; Jorgensen et al. , 2007;
Jørgensen et al. , 2009; Sharpe et al. , 2012). Fishing
practices and predation are usually non-random factors, as gears are
often designed to selectively take larger and older fish in the
population (Law, 2000). In this case, smaller fish are likely to have a
higher probability of survival than the larger ones, and among them,
those that can mature and reproduce early will be selected (Jorgensenet al. , 2007; Jørgensen et al. , 2009). Assuming that early
maturation is heritable to some extent, this should result in life
histories changing towards earlier reproduction at smaller sizes (Heathet al. , 2002; Olsen et al. , 2004; Ayllon et al. ,
2015; Sinclair-Waters et al. , 2020).
Parasitism can also affect the future reproductive success of hosts
(Fredensborg and Poulin, 2006) and thus select for changes in host life
history traits (Lafferty, 1993b; Perrin et al. , 1996; Sorciet al. , 1996; Yan et al. , 1997; Polak and Starmer, 1998;
Adamo, 1999; Agnew et al. , 1999; McCurdy et al. , 1999;
Richner and Tripet, 1999; Thomas et al. , 2000). For instance, an
increase in the prevalence of parasites causing castration (i.e.,destruction or alteration of the host’s gonadal tissues by the parasite;
(Noble and Noble, 1971) can select for earlier maturity (Minchella and
Loverde, 1981; Lafferty, 1993a; Loot et al. , 2002; Fredensborg
and Poulin, 2006). For the infected host, achieving reproduction prior
to castration yields clear fitness benefits (Minchella and Loverde,
1981; Lafferty, 1993a; Gooderham and Schulte-Hostedde, 2011), and these
benefits increase along with infection risk (Minchella and Loverde,
1981; Sorci et al. , 1996; Polak and Starmer, 1998). Increased
reproductive effort in hosts exposed to castrating parasites has been
reported in a number of species. So far, however, most documented life
history changes seem to result from adaptive plastic responses of hosts
to parasitic exposure, more than life history evolution following a
change in parasite-mediated selection (Chadwick and Little, 2005; Vale
and Little, 2012; Hudson et al. , 2019).
In this study, we investigated whether the castrating parasitic cestodeLigula intestinalis was responsible for a life history change in
the cyprinid fish Engraulicypris sardella in Lake Nyasa. We
studied the freshwater fish E. sardella , which is the second
intermediate host for the cestode L. intestinalis . E.
sardella (Günther, 1868), locally known as Usipa or Lake Malawi
sardine, is a small, slender, silvery, zooplanktivourous fish endemic to
Lake Nyasa (Rufli and Van Lissa, 1982; Lowe‐McConnell, 1993) that occurs
in shoals, which are widely distributed within the lake and found in
both near-shore areas and offshore pelagic water, down to a depth of
approximately 200 m (Maguza-Tembo et al. , 2009).
E. sardella is an annual species, where hatchlings grow and age
to reproduce and die in a yearly cycle (Iles, 1960), although some
studies indicate that they can live longer (Thompson and Bulirani, 1993;
Rusuwa et al. , 2014). They have been reported to breed throughout
the year but with bi-annual recruitment peaks occurring during the wet
season and dry season (Morioka and Kaunda, 2005; Rusuwa et al. ,
2014).
During early developmental stages E. sardella feeds exclusively
on phytoplankton, then switches to feeding on zooplankton upon reaching
adulthood (Degnbol, 1982; Allison et al. , 1996). E.
sardella demonstrates a rapid growth rate and can attain a maximum
total length of about 130 mm in a year (Tweddle and Lewis, 1990;
Thompson, 1996). Males and females mature at a size of about 70 and 75
mm respectively (Thompson et al. , 1996; Thompson and Allison,
1997).
E. sardella forms an important part of the food web of Lake
Nyasa. The species is primary consumer of zooplankton (Degnbol, 1982;
Konings, 1990), and an important prey for pelagic piscivorous fishes,
particularly Diplotaxodon spp. and Rhamphochromis spp.
(Allison et al. , 1996), as well as piscivorous birds (Linn and
Campbell, 1992). E. sardella is also of high commercial value,
and for many decades it has been the main animal protein source for most
of the local human population (Manyungwa-Pasani et al. , 2017).
However, recently it has been observed that these cyprinids are infected
by the cestode L. intestinalis .
L. intestinalis (L. 1758) is a common and widespread cestode,
that uses cyprinid fish as the second intermediate host (Kennedy, 1974;
Dubinina, 1980). The parasite is trophically transmitted and has a
complex life cycle involving two aquatic intermediate hosts, a
planktonic copepod and a fish (Dubinina, 1980; Loot et al. ,
2001). It reaches sexual maturity in the abdominal cavity of piscivorous
birds that are the final hosts (i.e., the hosts where parasite
reproduction takes place) (Dubinina, 1980; Loot et al. , 2001). In
infected fish the parasite is found filling the body cavity (Hooleet al. , 2010). Higher infection rates are observed in larger and
older E. sardella than in juvenile individuals (Msafiri et
al. , 2014; Rusuwa et al. , 2014), which can partly be explained
by diet shifts from phytoplankton to zooplankton as E. sardellareaches maturity.
The invasion of L. intestinalis in Lake Nyasa was first noted in
the late 1990s during long-line research surveys where a milkish white
worm was found in the body cavity of the endemic pelagic cyprinid fishE. sardella (Mwambungu et al. , 1996). The worm was
identified to be the tapeworm Ligula intestinalis (L.). This
parasite is believed to be introduced into Lake Nyasa by migrating
fish-eating birds such as the White-breasted cormorant
(Phalacrocorax carbo ), which is one of the most abundant
fish-eating birds in the Lake Nyasa basin (Linn and Campbell, 1992) and
one of the final hosts of L. intestinalis (Rosen, 1920; Lootet al. , 2001). In Lake Nyasa this cestode has been increasingly
reported since it was first noted by Mwambungu et al. (1996).E. sardella appears to be the only species used as intermediate
fish host (Msafiri et al. , 2014; Rusuwa et al. , 2014;
Gabagambi and Skorping, 2018; Gabagambi et al. , 2019)
(Supplementary Figure S1).
L. intestinalis is known to induce castration in several
intermediate hosts (Wyatt and Kennedy, 1988; Kennedy et al. ,
2001; Loot et al. , 2002; Cowx et al. , 2008; Hoole et
al. , 2010) and has therefore been suggested to cause population crashes
of its host (Burrough et al. , 1979; Kennedy et al. , 2001).
This could sometimes lead to local extinction of the parasite in small
ecosystems (Kennedy et al. , 2001). Recent results, however,
indicate that local extinction of this parasite is unlikely in Lake
Nyasa due to spatial and temporal variations in transmission rates
(Gabagambi and Skorping, 2018).
Under such conditions of recent invasion, we hypothesize that the
cestode L. intestinalis should select for a shift in resource
investment from somatic growth towards reproduction in its intermediate
fish host E. sardella . Using data collected from 2005 to 2015 in
the northern part of Lake Nyasa, we address the following three
questions:
(i) What are the effects of L. intestinalis on the fecundity ofE. sardella ? (ii) has reproductive investment at maturity ofE. sardella increased over time? and (iii) has the average size
at maturity of E. sardella decreased?
We then further discuss the selective roles of parasitic invasionversus other environmental factors that may recently have changed
in Lake Nyasa.