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Two's a crowd? Crowding effect in a parasitic castrator drives differences in reproductive resource allocation in single vs double infections

Published online by Cambridge University Press:  08 December 2016

CAITLIN R. FONG Open the ORCID record for CAITLIN R. FONG [Opens in a new window] ,
NANCY A. MORON  and
ARMAND M. KURIS
CAITLIN R. FONG*
Affiliation:
Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge, CA 91330, USA
NANCY A. MORON
Affiliation:
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA
ARMAND M. KURIS
Affiliation:
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA
*
*Corresponding author. Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge, CA 91330, USA. E-mail: cat.r.fong@gmail.com
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Summary

The ‘crowding effect’ is a result of competition by parasites within a host for finite resources. Typically, the severity of this effect increases with increasing numbers of parasites within a host and manifests in reduced body size and thus fitness. Evidence for the crowding effect is mixed – while some have found negative effects, others have found a positive effect of increased parasite load on parasite fitness. Parasites are consumers with diverse trophic strategies reflected in their life history traits. These distinctions are useful to predict the effects of crowding. We studied a parasitic castrator, a parasite that usurps host reproductive energy and renders the host sterile. Parasitic castrators typically occur as single infections within hosts. With multiple parasitic castrators, we expect strong competition and evidence of crowding. We directly assess the effect of crowding on reproductive success in a barnacle population infected by a unique parasitic castrator, Hemioniscus balani, an isopod parasite that infects and blocks reproduction of barnacles. We find (1) strong evidence of crowding in double infections, (2) increased frequency of double infections in larger barnacle hosts with more resources and (3) perfect compensation in egg production, supporting strong space limitation. Our results document that the effects of crowding are particularly severe for this parasitic castrator, and may be applicable to other castrators that are also resource or space limited.

Keywords

parasitic castratorcrowding effectparasite ecologyHemioniscus balaniChthamalus fissusrocky intertidal
Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 662 - 668
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Copyright
Copyright © Cambridge University Press 2016 

INTRODUCTION

The ‘crowding effect’ is a prime example of competition (Bush and Lotz, Reference Bush and Lotz2000; Roberts, Reference Roberts2000). This effect occurs when there are multiple parasites within a host competing for finite resources. The crowding effect often results in a decreased mean parasite body size, and thus decreased individual fitness, as the number of parasites within a single host increases (Read, Reference Read1951; Holmes, Reference Holmes1961; Bush and Lotz, Reference Bush and Lotz2000). Crowding can also result in spatial displacement of parasites within the host due to competition for attachment sites (Holmes, Reference Holmes1961). These competitive interactions have important implications for parasite fitness and may regulate parasite populations (Holmes, Reference Holmes1961; Brown et al. Reference Brown, De Lorgeril, Joly and Thomas2003; Fredensborg and Poulin, Reference Fredensborg and Poulin2005; Heins and Baker, Reference Heins and Baker2011; Pollitt et al. Reference Pollitt, Churcher, Dawes, Khan, Sajid, Basáñez, Colegrave and Reece2013). Crowding of parasites within hosts has been used to explore both inter- and intra- specific competition, and has provided useful insight into parasite competitive interactions (e.g. Holmes, Reference Holmes1961, Reference Holmes1962a , Reference Holmes b ; Heins et al. Reference Heins, Baker and Martin2002; Poulin et al. Reference Poulin, Giari, Simoni and Dezfuli2003; Lowrie et al. Reference Lowrie, Behnke and Barnard2004; Fredensborg and Poulin; Reference Fredensborg and Poulin2005; Serafim et al. Reference Serafim, da Silva, de Paiva, dos Santos, Silva, Carneiro, Dias and Rabelo2014). Empirical evidence for competition is mixed – while some researchers have found a strong correlation between increased parasite load and decreased mean parasite size, others have found no relationship or even a positive relationship (for negative crowding effects, see Holmes, Reference Holmes1961, Reference Holmes1962a ; Lalonde and Roitberg, Reference Lalonde and Roitberg1992; Reitz, Reference Reitz1995; Desouhant et al. Reference Desouhant, Debouzie, Ploye and Menu2000; Heins et al. Reference Heins, Baker and Martin2002; Brown et al. Reference Brown, De Lorgeril, Joly and Thomas2003; Poulin et al. Reference Poulin, Giari, Simoni and Dezfuli2003; Lowrie et al. Reference Lowrie, Behnke and Barnard2004; Fredensborg and Poulin, Reference Fredensborg and Poulin2005; Keasar et al. Reference Keasar, Segoli, Barak, Steinberg, Giron, Strand, Bouskila and Harari2006; Serafim et al. Reference Serafim, da Silva, de Paiva, dos Santos, Silva, Carneiro, Dias and Rabelo2014 for lack of a crowding effect, see Holmes, Reference Holmes1962b ; Poulin et al. Reference Poulin, Giari, Simoni and Dezfuli2003; for a positive effect of crowding see Kuris, Reference Kuris2003, Reference Kuris2005; Weinersmith et al. Reference Weinersmith, Warinner, Tan, Harris, Mora, Kuris, Lafferty and Hechinger2014).

The nature of the explicit parasitic trophic strategy may predict the effects of crowding. Parasites can be divided into 7 distinctive consumer strategies (Kuris and Lafferty, Reference Kuris, Lafferty, Poulin, Morand and Skorping2000; Lafferty et al. Reference Lafferty, DeLeo, Briggs, Dobson, Gross and Kuris2015). For each, their underlying commonality of life histories associated with each trophic strategy may help explain the diverse responses to increased parasite load (see Table 1 for examples). For example, most studies on crowding have been done in the final host for helminth intestinal parasites, which are macroparasites (Lafferty et al. Reference Lafferty, DeLeo, Briggs, Dobson, Gross and Kuris2015) (=typical parasites sensu Lafferty and Kuris, Reference Lafferty and Kuris2002). For these parasites, adults live and reproduce in the host, making competition for resources likely. Competition among macroparasites has been demonstrated for both space and nutrients (Holmes, Reference Holmes1961, Reference Holmes1962a , Reference Holmes b ; Serafim et al. Reference Serafim, da Silva, de Paiva, dos Santos, Silva, Carneiro, Dias and Rabelo2014). Crowding can have an additional consequence for typical parasites; in some cases, crowding results in smaller parasite sizes, which produce fewer eggs, limiting the parasite's ability to successfully infect the next host (e.g. Heins et al. Reference Heins, Baker and Martin2002). Similarly, competition can be strong for parasitoids, where the offspring develop within a host that dies once the parasites reach maturity (sensu Lafferty and Kuris, Reference Lafferty and Kuris2002). Competition for host resources can be intense for parasitoids because the body of the host is finite and consumed by the end of the interaction (reviewed in Lafferty and Kuris, Reference Lafferty and Kuris2002; Harvey et al. Reference Harvey, Poelman and Tanaka2013). Trophically transmitted parasites, parasites that must be consumed while in an intermediate host to reach the final host (Lafferty and Kuris, Reference Lafferty and Kuris2002), often experience a crowding effect (Brown et al. Reference Brown, De Lorgeril, Joly and Thomas2003; Fredensborg and Poulin, Reference Fredensborg and Poulin2005) though recent evidence indicates this is not universal (Weinersmith et al. Reference Weinersmith, Warinner, Tan, Harris, Mora, Kuris, Lafferty and Hechinger2014). In some cases, trophically transmitted parasites are substantially smaller than their host, making resource competition less likely (e.g. Weinersmith et al. Reference Weinersmith, Warinner, Tan, Harris, Mora, Kuris, Lafferty and Hechinger2014); in fact, an increase in the number of parasites may increase transmission rates, particularly if transmission is enhanced by parasite-induced changes in prey host behaviour that promote transmission to the predator host (e.g. Lafferty and Morris, Reference Lafferty and Morris1996; Kuris, Reference Kuris2003). In this study, we examine a parasitic castrator, a parasite that usurps host reproductive energy and renders the host sterile (sensu Lafferty and Kuris, Reference Lafferty and Kuris2002). Parasitic castrators are typically found in a 1:1 ratio with their host, which is likely due to competitive exclusion (Lafferty and Kuris, Reference Lafferty and Kuris2009). Thus, in cases with multiple parasitic castrators, we expect strong competition and evidence of crowding.

Table 1. Examples of empirical evidence for the crowding effect for some parasite functional groups (pathogens are not included).

We investigate crowding in a barnacle population infected by a unique parasitic castrator. Hemioniscus balani is an isopod parasite that infects and castrates at least 11 species of barnacle (Crisp, Reference Crisp1968; Blower and Roughgarden, Reference Blower and Roughgarden1988). Hemioniscus balani is a sequential hermaphrodite – the parasite enters the barnacle as a male and then metamorphoses into a female. The second parasite to enter as a male, fertilizes the female and then leaves the barnacle host. Hemioniscus balani enters the barnacle, attaches to the ovaries, consuming ovarian fluid; thus, the barnacle is unable to reproduce as a female though male function is retained in hermaphroditic hosts. Thus, a barnacle infected by a single parasitic castrator is unable to reproduce as a female while infected (Lafferty and Kuris, Reference Lafferty and Kuris2009). After the isopod matures, it releases its offspring and then dies, leaving the host alive and able to recover female functionality; hence, it is an ephemeral semelparous parasitic castrator.

In this study, we directly assess the effect of crowding on the reproductive success of H. balani. We predict strong competition because (1) H. balani feeds on ovarian fluid, a likely limiting resource, and (2) the barnacle host has a hard test, offering a finite amount of space for such a parasite. We predict that both of these probable constraints will strongly control parasite egg production and drive competition in doubly infected barnacle hosts.

METHODS AND MATERIALS

We surveyed a natural population of the intertidal barnacle, Chthamalus fissus, at Coal Oil Point, Santa Barbara, CA to determine the relationship between length of the host barnacle and the probability of it being uninfected, infected with a single parasite, or infected with two female parasites of the isopod parasite, H. balani. We sampled all barnacles encountered within a 5 × 5 cm2 plot on 06 July 2015 and immediately froze the sample for later dissection in the laboratory. Barnacles were collected from a single location because prevalence of this parasite does not depend on local host density or aggregation (Fong, Reference Fong2016). Each barnacle host was measured to the nearest ¼ mm along its longest diameter, scored for infection and categorized as uninfected, infected by a single parasite, or infected by more than one parasite. We conducted a logistic regression with length as the predictor variable and infection status as the response variable to determine the relationship between barnacle length and infection status (uninfected, infected by a single parasite, or infected by more than one parasite).

To determine if egg production by a single parasite was significantly different from total egg production in a double infection, we collected hosts from Coal Oil Point July–September 2015 and froze them for dissection in the laboratory. As before, we dissected barnacles and measured each host length to the nearest ¼ mm. We then determined whether the barnacle was infected by one or two parasites. We isolated and dissected the parasites, under a stereomicroscope, and counted the number of eggs. To minimize differences in timing of the double infections or differences in development rates, we only counted the eggs in fully mature parasites (defined by the presence of developed eggs). In double infections, we only included hosts with fully mature parasites to minimize differences due to parasite maturity. Because egg production may be strongly limited by the space inside of the barnacle, we converted length to volume and approximated barnacle volume as a half sphere [(V = 4/3πr 3)/2]. We then used a regression approach to determine if there was a significant difference in egg production within barnacles infected by a single parasite vs two parasites.

We dissected 59 barnacles with a single mature parasite and 55 barnacles with two mature parasites and counted the number of eggs within each parasite. Barnacle length ranged from 2 to 6·75 cm. To determine if there was unequal competition between the two parasites in a double infection, and to determine if this relationship varied with size, we used a multiple regression approach to determine if there was a significant difference in egg production between the more and the less productive parasite (hereafter called the larger and smaller parasite).

RESULTS

We dissected 403 barnacles, of which 61% were uninfected, 36·7% were infected with a single parasite and 7·9% were infected with two parasites. In the single infections, 34·5% of the parasites were mature. However, only 2·2% of the barnacle hosts were infected by two mature female parasites. No triple infections were observed.

The probability of being uninfected, infected with a single parasite and infected by more than one parasite depended on the size of the barnacle host (Fig. 1), with a significant relationship between length and infection status (Logistic regression, chi square = 70·5, length P < 0·0001). The probability of being infected increased with size such that the largest size class of barnacles had greater than a 60% chance of being infected. Further, the probability of infection increased with size, though with different patterns for single vs double infections. The probability of being infected by a single parasite was maximal at 4 mm. In contrast, the probability of being infected by two female parasites increased with barnacle host size over the size range of the barnacles. Thus, the largest size class of barnacles had ~6% chance of being uninfected, ~55% chance of being infected by a single parasite and ~39% chance of being infected by more than one parasite.

Fig. 1. Size frequency distribution of single and multiple (2+) infections (n = 403). Bars are count data while lines are probability equations derived from the logistic regression. White bars are uninfected individuals, grey bars are singly infected individuals and black bars are double infections. The solid line is the predicted probability of being uninfected, the dotted line is the predicted probability of having a single parasite and the dashed line is the probability of having two parasites.

The total number of eggs produced by parasites as a function of barnacle host length was not significantly different for single vs double infections (Fig. 2). Our multiple regression analysis indicated only barnacle length significantly affected parasite egg production, thus number of parasites was dropped from the regression (linear regression, F(1,112) = 12·8, P = 0·0005, R 2 = 0·10). Thus, regardless of number of parasites, total egg production was equivalent and parasites in larger hosts produced more eggs (y = 0·9875x + 70·779).

Fig. 2. Relationship between barnacle volume and parasite egg production. Black points are data from hosts with a single parasite while white dots are data from hosts with two parasites.

We found a significant interaction between parasite size and barnacle size (multiple regression, F(3,106) = 33·2, interaction P = 0·0497). Hence, a larger parasite makes more eggs than does a smaller parasite, and this difference increases with host size (Fig. 3). Egg production of the larger parasite has a significant but weak relationship to barnacle host size (linear regression, F(1, 53) = 4·6, P = 0·0365, y = 0·54x + 57·08, R 2 = 0·08). However, egg production of the smaller parasites does not have a significant relationship with barnacle host size (linear regression, F(1,53), P = 0·80). Thus, the larger parasite is able to convert a larger host body size to its own egg production while the smaller parasite cannot gain a similar advantage. On average, in double infections the larger parasite produced the majority, 70·1 ± 1·4%, of the eggs, more than twice as many eggs as did the smaller parasite.

Fig. 3. Number of eggs produced by the larger (black) and smaller (white) parasite in a double infections. Bars are means ± s.d..

DISCUSSION

We find strong evidence for a crowding effect for H. balani in Chthamalus fissus. Because a single castrator can generally consume all of the host's reproductive energy (Lafferty & Kuris, Reference Lafferty and Kuris2002, Lafferty and Kuris, Reference Lafferty and Kuris2009), there is a strong propensity to manifest intense competition and double infections are usually quite rare. Generally, the dispersion of parasitic castrators in the host population is close to uniform with a mode and mean of 1, which underscores the severity of competition between parasites (Kuris, Reference Kuris1974; Lafferty and Kuris, Reference Lafferty and Kuris2009). The scarcity of multiple infections has been documented in several instances. In a survey of 12 033 fiddler crabs for bopyrid isopods, 9·2% were infected, yet only 0·07% were infected by two adult females (Roccatagliata and Jordá, Reference Roccatagliata and Jordá2002). Further, for an entoniscid isopod parasite of shore crabs, 1 mature female is typical and only at sites with high prevalence (>70%) are infections with two or more mature females common (Kuris et al. Reference Kuris, Poinar and Hess1980; Lafferty and Kuris, Reference Lafferty and Kuris2009). Additionally, a survey of cymathoid isopods on 248 cardinal fish never found more than 1 adult parasite on a fish (Fogelman et al. Reference Fogelman, Kuris and Grutter2009). However, parasitic castrators are not always found in a 1:1 ratio with their hosts. In a survey of a barnacle parasitic castrator of crabs, Hartnoll (Reference Hartnoll1967) found high incidence of multiple parasites in a single host for one species (60%) but not the other (0·8%). In the cases of multiple castrators, a crowding effect was evident – the externa of the parasite decreased in size with increased numbers of parasites (up to 5). In this study, we found 2 mature female parasites in 2·2% of the hosts surveyed. This rarity of multiple parasitic castrators within a single host suggests a strong and active mechanism for prevention, mediated either by the host or the parasite.

We suggest the rarity of double infections likely resulted from host choice. Hemioniscus balani has a highly mobile searching stage that appears to have a behavioural repertoire capable of host discrimination. Unfertilized female parasites must be located and fertilized by males, suggesting that the infectious stage is highly mobile and capable of host discrimination. This mobility and its searching ability may enable rejection of already parasitized hosts. This has some similarities to searching by insect parasitoids where mobile searching adult females are capable of selecting hosts and rejecting already parasitized individuals (e.g. Hofsvang, Reference Hofsvang1988; Lalonde and Roitberg, Reference Lalonde and Roitberg1992; Keasar et al. Reference Keasar, Segoli, Barak, Steinberg, Giron, Strand, Bouskila and Harari2006). Alternately, double infections generally resulted from near simultaneous infections, as appears to be the case for bopyrid isopods (reviewed in Lafferty and Kuris, Reference Lafferty and Kuris2009). However, the wide range of multiple infections and the wide variation in their stages of development in this study indicate that presence of early infections does not block arrival of later infections and that their sizes (the later arrivals) are due to suppression by the early arrivals. We find it more likely, double infections are rare because the presence of one parasite deterred the second parasite. We find this more likely because the smaller parasite has reduced egg production compared with the large parasite, which is likely a sufficient deterrent to the second parasite. While the sensory and motor capabilities of a cryptoniscus larva are unlikely to match those of adult parasitoids, the mobile infectious stage found in this parasite may provide a mechanism for the rarity of double infections. We suggest that cryptoniscus larvae may have sensory capabilities adequate to detect host infection status, and that since barnacles are usually aggregated in dense clusters, more suitable hosts will often be nearby.

Double infections were more common in large barnacles. Larger hosts are usually more parasitized than are smaller hosts, despite the often more competent defensive systems of larger hosts (for review see Combes, Reference Combes2001). One explanation is larger hosts have a greater probability of encounter parasites simply due to their larger size (e.g. Poulin et al. Reference Poulin, Curtis and Rau1991). However, age often covaries with size, and older individuals have had increased exposure to parasites hosts, making discriminating between these two explanations challenging. Here, we think it unlikely that parasitism relates to host age, because the parasite is short-lived (estimated at 10 days, Blower and Roughgarden, Reference Blower and Roughgarden1987) and the barnacle host recovers following infection. Hence, we suggest that as the number of available hosts decreases, parasites may make the best of a bad situation and infect already infected large hosts.

While we are unable to elucidate the mechanism for this crowding effect, the strong compensation in total parasite egg production suggests that the parasites are space limited. Single and double infections resulted in statistically equivalent total egg production despite the unequal reproductive success of the two parasites, and that parasite egg production was constrained by barnacle length. Thus, we find direct competition for space to be the most likely mechanism resulting in the crowding effect.

Our evidence does not support other possible competitive mechanisms such as direct competition for nutrients, indirect competition via toxin production, or mediation by host immunity as causal factors. Research on crowding for other parasite systems supported strong evidence for nutrient limitation, and this type of limitation results in smaller individuals, immature females and reduced fecundity (Holmes, Reference Holmes1961, Reference Holmes1962a , for review see Lafferty and Kuris, Reference Lafferty and Kuris2009). The frequent presence of 2 fully mature females in double infections with summed equivalent egg production to a single parasite suggested that nutrient limitation did not stunt net productivity of the parasites. We found no evidence for toxin production, as parasites were not spatially displaced within the host in double infections nor had one parasite killed the other. Finally, we find no evidence of competition mediated by host immunity because there was no evidence of melanization, the immune response of crustaceans (Kuris et al. Reference Kuris, Poinar and Hess1980; Götz, Reference Götz and Brehélin1986). Thus, competition for space is the most plausible and parsimonious mechanism for the observed crowding effect.

We found a weak positive relationship for parasite egg production on host barnacle size, whereas for other parasitic castrators, parasite body size and parasite fecundity scale strongly with host size (Munoz and George-Nascimento, Reference Munoz and George-Nascimento1999; Kuris and Lafferty, Reference Kuris, Lafferty, Poulin, Morand and Skorping2000; Hechinger et al. Reference Hechinger, Lafferty, Mancini, Warner and Kuris2009). However, H. balani is a unique castrator in that it is not long-lived; a modelling approach estimated H. balani may live an average of about 10 days in Balanus glandula (Blower and Roughgarden, Reference Blower and Roughgarden1989). Because H. balani is short lived, it may not grow with positive allometry as the host grows. Tracking host growth is a common life history feature of other castrators (e.g. Fogelman et al. Reference Fogelman, Kuris and Grutter2009). The inability of this ephemeral parasite to grow along with it host may be what weakened its relationship between host size, and consequently the size-dependent relationship with parasite egg production.

In sum, we find (1) strong evidence of crowding in double infections for a parasitic castrator, (2) increased double infections in larger barnacle hosts with more resources and (3) strong compensation in parasite egg production for double infections, supporting space limitation as the driver for fecundity of H. balani in its barnacle host.

ACKNOWLEDGEMENTS

We would like to thank the Ecological Parasitology group at UCSB for support, discussion and valuable insight. C.R.F. would like to thank her Ph.D. dissertation committee for valuable support.

FINANCIAL SUPPORT

We thank NSF EEID grant (OCE-1115965) for support.

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Figure 0

Table 1. Examples of empirical evidence for the crowding effect for some parasite functional groups (pathogens are not included).

Figure 1

Fig. 1. Size frequency distribution of single and multiple (2+) infections (n = 403). Bars are count data while lines are probability equations derived from the logistic regression. White bars are uninfected individuals, grey bars are singly infected individuals and black bars are double infections. The solid line is the predicted probability of being uninfected, the dotted line is the predicted probability of having a single parasite and the dashed line is the probability of having two parasites.

Figure 2

Fig. 2. Relationship between barnacle volume and parasite egg production. Black points are data from hosts with a single parasite while white dots are data from hosts with two parasites.

Figure 3

Fig. 3. Number of eggs produced by the larger (black) and smaller (white) parasite in a double infections. Bars are means ± s.d..