Introduction
There is increasing attention on the dilution effect of biodiversity on
infectious
diseases.
The dilution effect hypothesis (DEH) suggests that high species
diversity in a community including low competent and incompetent hosts
can reduce risk of infectious disease (Ostfeld & Keesing 2000).
Encounter (contact) reduction, transmission reduction (following
encounters), and susceptible host regulation were proposed as underlying
mechanisms of the DEH (Keesing et al. 2006; Ostfeld & Keesing
2012), although altered susceptibility due to stressors may also play a
role (Buss & Hua 2023). However, the generality of the DEH remains
controversial given that increasing host species also introduces more
pathogens in complex systems (Randolph & Dobson 2012; Wood & Lafferty
2013; Wood et al. 2014). Meta-analysis suggested that the
magnitude of the dilution effect on plant diseases varied between
ecosystem type, pathogen type, study design (observational versus
manipulative), parasite life history and latitude (Liu et al.2020). In contrast, the magnitude of the dilution effect on zoonotic
diseases was independent of host density, study design, and type and
specialization of parasites, but related to the relative abundance of
the focal host (Civitello et al. 2015). Therefore, in addition to
identifying patterns using correlative studies, mechanisms should be
experimentally tested in different disease systems to determine when and
where the DEH occurs (Halsey 2019).
A meta-analysis of published studies revealed that the dilution effect
occurs commonly on plant, wildlife and human diseases (Civitelloet al. 2015). The DEH also has been observed in aquatic
host-parasite systems involving anuran, teleost and molluscan hosts
infected with fungal, monogenean and trematode parasites (Johnsonet al. 2008; Thieltges et al. 2008; Johnson & Hartson
2009; Johnson et al. 2009; Johnson & Hoverman 2012; Dargentet al. 2013; Venesky et al. 2014; Gendron & Marcogliese
2017). The occurrence of a dilution effect may rely on the specific
composition of the host community (Johnson et al. 2013; Salkeldet al. 2013), as variation in host quality is a condition
necessary for reduction in pathogen transmission (Keesing & Ostfeld
2021a).
Encounter reduction, considered one of the most common mechanisms behind
the dilution effect (Johnson & Thieltges 2010), may occur via a number
of means, including mortality of free-living parasite stages, mortality
of parasitic stages on hosts, or alterations in host behavior and
activity (Johnson & Thieltges 2010). Changes in host behavior may
affect the likelihood of parasite encounter and subsequent risk of
infection (Johnson & Thieltges 2010). For example, the presence of
predators affects anticercarial behavior in tadpoles, contributing to
the increase in exposure rates to trematode parasites (Rohr et
al. 2015). Sex differences in the degree of shoaling behavior and
inter-individual contact rates determines relative infection levels ofGyrodactylus turnbulli in the guppy (Poecilia reticulata )
males and females (Richards et al., 2010). Given that shoaling behavior
in guppies affects transmission of gyrodactylids (Richards et al., 2010;
Johnson et al., 2011), any changes in schooling behavior will likely
affect the risk of infection. How one fish species with schooling
behavior responds to the presence of other fish species may then result
in the occurrence of a dilution effect. However the effects of host
schooling on the occurrence of the dilution effect have never been
tested in previous empirical studies and predictive models.
The monogenean Gyrodactylus kobayashii is the most common
gyrodactylid on ornamental goldfish (Carassius auratus ) (Liet al. 2014), and the goldfish-G. kobayashii model has
been established to study the transmission of the parasite under
laboratory conditions (Zhou et al. 2017). While monogeneans tend
to show high specificity to a particular host, gyrodactylids are known
to infect other host species under experimental conditions, albeit with
low infection success (King & Cable 2007; King et al. 2009). The
viviparous gyrodactylids mainly transmit via contact between hosts, and
have the capability of continuous transmission during their entire
lifetime (Boeger et al. 2005).
Using this system, we first determined if host competence was a
necessary condition for the dilution effect to occur in the
goldfish-G. kobayashii model system. To test the influence of
host competence on parasite transmission, we added other fish species of
varying competence to the experimental system. This experiment also
examined effects of host diversity and abundance on transmission.
Goldfish display schooling behavior, and mean distance among individuals
and schooling pattern varies with the population size of goldfish (Leemet al. 2012; Jeon et al. 2013). Importantly, the frequency
of social contact affects gyrodactylid transmission in guppies (Johnsonet al. 2011). We thus examined if schooling behavior in goldfish
plays a role in parasite transmission and, potentially, the occurrence
of the dilution effect in the presence of other host species of varying
competence.