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.