In salt marsh ecosystems, daggerblade grass shrimp, Palaemon (Palaemonetes) pugio, play a crucial role in food webs and serve as the definitive host for the bopyrid isopod Probopyrus pandalicola. These ectoparasites infest the branchial chambers of grass shrimp, which can lead to decreased energy availability and sterilization of infected hosts. Although bopyrid isopod infestation of daggerblade grass shrimp has been frequently reported in literature from coastal marshes of the southeastern United States, the prevalence of this parasite has not been recently documented in daggerblade grass shrimp from marshes of the northeastern United States. The goal of this project was to quantify the prevalence of Pr. pandalicola infestations in Pa. pugio across Cape Cod, Massachusetts. We evaluated bopyrid isopod prevalence from shrimp collected from 5 different salt marsh habitats along Cape Cod in August 2021. Bopyrid isopod infestations were found in shrimp at 4 of 5 salt marshes, with prevalence ranging from 0.04 to 14.1%. Seasonal resampling of one of the salt marshes revealed the highest average infestation prevalence in spring (<17.1%) and an isolated high of 30.3% prevalence in a single salt panne. A series of linear and multivariate models showed that panne area, shrimp abundance, and distance to shoreline were related to Pr. pandalicola shrimp infestations in salt pannes in summer. This study describes the prevalence of the bopyrid isopod infesting daggerblade grass shrimp in salt marshes in New England, with implications for how parasitized shrimp influence salt marsh food webs in which they are found.

Parasites are ubiquitous in nearly all ecosystems and phyla (Dobson et al., 2008), and parasitic plants and animals play a large role in structuring host populations, usually by negatively influencing host fitness as parasites rely on hosts for refuge, nutrition, and/or mobility (Pennings and Bertness, 2001; Hatcher and Dunn 2011; Welicky and Sikkel, 2014). In salt marshes, parasites play an important role in influencing population, community, and even ecosystem dynamics (Lafferty et al., 2006; Morton and Silliman, 2020). For instance, some parasitic salt marsh plants may negatively influence host plant abundance and distribution by depleting nutrients from their hosts (Pennings and Bertness, 2001). In one recent study, trematode parasites of marsh periwinkle snails (Littoraria irrorata) from North Carolina marshes were experimentally reduced and salt marsh plants subsequently declined, indicating that parasite prevalence may indirectly benefit salt marsh plants and potentially increase their resistance to overgrazing in the face of prolonged drought (Morton and Silliman, 2020). Additionally, parasites have been shown to affect community structure by infesting multiple species in salt marsh food webs, influencing the number of trophic links and food web connectance (Lafferty et al., 2006). Although parasites in salt marshes are abundant and play an important ecological role, prevalence data on parasites and host-parasite interactions generally remain lacking (Dobson et al., 2008; Welicky and Sikkel, 2014). This may partially be explained by the cryptic nature of parasites (Roche et al., 2013), although many ectoparasites are fairly conspicuous, even post-infection (Roche et al., 2013).

Parasitic isopods are a common group of crustaceans and can act as ectoparasites on several taxa (Leonardos and Trilles, 2003; Welicky and Sikkel, 2014) including salt marsh shrimp species, such as the ecologically important daggerblade grass shrimp (Palaemon [previously Palaemonetes] pugio; see De Grave and Ashelby, 2013). Daggerblade grass shrimp are endemic to salt marshes along the western Atlantic and throughout the Gulf of Mexico (Welsh, 1975; Collins, 1981; Anderson, 1985). Palaemon pugio, hereafter referred to as grass shrimp, plays a critical role in salt marsh food webs as prey for a variety of shorebirds, crabs, and finfish, including commercially important species (Heard and Lutz, 1982; Manderson et al., 2000). Depending on their life stage and food availability, grass shrimp act as opportunistic omnivores or detritivores, influencing multiple trophic levels (Welsh, 1975; McCall and Rakocinski, 2007). Additionally, grass shrimp influence salt marsh structure, functioning, and dynamics through their feeding behavior and movement. For instance, grass shrimp can indirectly increase macrophyte productivity by grazing on epiphytes that inhibit photosynthetically active radiation and can also increase nutrient availability to macrophytes and microbes via bioturbation and fecal deposition (Welsh, 1975; Sikora, 1977; McCall and Rakocinski, 2007).

Grass shrimp serve as definitive hosts of the bopyrid isopod Probopyrus pandalicola (Packard, 1879), an ectoparasite found in female-male pairs in the shrimp’s branchial chambers (Anderson, 1977). After Pr. pandalicola have parasitized their intermediate hosts (calanoid copepods), the first parasite to settle on the host grass shrimp will metamorphose into a female, and the second parasite to settle will become male (Baeza et al., 2018). Bopyrid isopod parasites remain on their hosts, growing with them even as their hosts molt (Cash and Bauer, 1993). The female isopod feeds on host hemolymph, consuming 1–10% of the total energy intake of the shrimp, reducing shrimp respiration, metabolism, and growth (Anderson, 1975, 1977; Ludwig, 2009). These parasites also castrate shrimp hosts and have been known to negatively influence host population size (Chaplin-Ebanks and Curran, 2007; Calado et al., 2008; Sherman and Curran, 2015). In addition to the direct effects that Pr. pandalicola have on grass shrimp, they also may influence shrimp behavior, resulting in altered movements and more conspicuous hosts, with possible implications for predator-prey dynamics (Bass and Weiss, 1999; Brinton and Curran, 2015a).

Probopyrus pandalicola have been observed from New Hampshire to São Paulo, Brazil (Richardson, 1904, 1905; Beck, 1979). However, although Pr. pandalicola have been commonly found on grass shrimp from salt marsh systems throughout the southeastern United States (Markham, 1985), observations noting Pr. pandalicola grass shrimp infestation in salt marshes north of Maryland have been less frequent, leaving a paucity of data regarding Pr. pandalicola infestation of estuarine grass shrimp in the northeastern United States (but see Kunkel, 1918 for records of Pr. pandalicola from Connecticut and Fowler, 1912 for records of Pr. pandalicola from New Jersey). In Massachusetts, Pr. pandalicola have been reported from the Ashcunet River in the early 1900s (Sumner et al., 1913). Additionally, 66 individual specimens of Pr. pandalicola were taken from Woods Hole, Massachusetts, in August 1950, and 7 additional individual specimens were documented from Buzzards Bay, Massachusetts, from January 1882 (Smithsonian National Museum of Natural History, USNM 91223, 91224, 91225, 39428). Although these reports are notable, the limited number of observations documenting Pr. pandalicola over the past century suggests either a low abundance or broad underreporting of these parasites in the Northeast, although the known observations and distribution of Pr. pandalicola may be obscured by their taxonomic complexity, with specimens initially identified as Pr. pandalicola (Markham, 1985), later differentiated into unique species (Ribeiro et al., 2019).

In the spring of 2019, Pr. pandalicola were observed on daggerblade grass shrimp in salt marshes on Cape Cod, Massachusetts (E. Stoner, pers. comm.). As such, we sought to provide an updated report on the prevalence of Pr. pandalicola from grass shrimp in salt marsh habitats on Cape Cod.

Sample locations

In August 2021 we collected grass shrimp from 5 salt marsh sites dispersed across Cape Cod: Wellfleet (41°56′15″N, 70°2′0″W), Yarmouth Port (41°42′17″N, 70°13′15″W), East Sandwich (41°44′16″N, 70°25′23″W), West Dennis (41°39′42″N, 70°9′43″W), and Cummaquid (41°43′12″N, 70°15′0″W; Fig. 1). Each site was dominated by a combination of the foundational salt marsh cordgrass (Spartina alterniflora) and/or salt marsh hay (Spartina patens) and was accessible by foot at low tide. Except for the Cummaquid site, grass shrimp were collected at the marsh’s edge from a single location within a perennial first-order stream (hereafter referred to as a tidal creek). Because there was no tidal creek at the Cummaquid site, we instead sampled 13 individual pannes (tide-pool-like depressions in the marsh) to investigate the distribution of both grass shrimp and Pr. pandalicola within these salt marsh microhabitats. The August 2021 sampling revealed a relatively high prevalence of Pr. pandalicola at the Cummaquid site, and as such, pannes were resampled in the fall (October 2021) and spring (March 2022) to examine shifts in shrimp and parasite abundance and shrimp infestation prevalence. However, because of the dynamic and seasonal nature of salt marsh pannes at this site, resampling the same pannes or even the same number of pannes was not always feasible. Therefore, we sampled 9 pannes in summer 2021 (Fig. 2A, pannes 6–14), 7 pannes in fall 2021 (Fig. 2A, pannes 1–7), and 7 pannes in spring 2022 (Fig. 2A, pannes 2–8). This sampling allowed for general comparisons of parasite prevalence by panne and season.

Figure 1.

Map showing bopyrid parasite prevalence in daggerblade grass shrimp observed in August 2021. Percent values showing bopyrid parasite Probopyrus pandalicola prevalence in daggerblade grass shrimp Palaemon pugio. Color version available online.

Figure 1.

Map showing bopyrid parasite prevalence in daggerblade grass shrimp observed in August 2021. Percent values showing bopyrid parasite Probopyrus pandalicola prevalence in daggerblade grass shrimp Palaemon pugio. Color version available online.

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Figure 2.

(A) Pannes sampled in Cummaquid, Massachusetts. Mean ± standard deviation (n = the total number of daggerblade grass shrimp collected) of Probopyrus pandalicola parasite prevalence for (B) each month and (C) across pannes. Color version available online.

Figure 2.

(A) Pannes sampled in Cummaquid, Massachusetts. Mean ± standard deviation (n = the total number of daggerblade grass shrimp collected) of Probopyrus pandalicola parasite prevalence for (B) each month and (C) across pannes. Color version available online.

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Sampling procedure

All sampling was completed at low tide. At each tidal creek site, salinity and temperature were recorded at the bottom water column (∼1 m) of the tidal creek directly adjacent to the sampling area using a YSI handheld device (YSI ProQuatro®, Xylem Brand, Yellow Springs, Ohio). At each site, shrimp were sampled following the modified protocol outlined in Hammerschlag-Peyer et al. (2013) in which submerged dip nets were swept through the water until 3 consecutive sweeps yielded fewer than 3 additional grass shrimp.

At the Cummaquid site, temperature and salinity measurements were taken, and shrimp were collected within each of the salt pannes sampled. Additionally, the length, width, and depth of each panne were recorded. Shrimp were then collected from a 3 × 1 m area within each panne; the panne area and distance to the shoreline were measured in Google Maps. Collected shrimp were transferred to plastic bags, placed on ice, and taken back to the lab at Bentley University, where samples were stored in a freezer until processed.

Processing procedure

Grass shrimp species were confirmed using available published keys (Anderson, 1985). The presence or absence of Pr. pandalicola was determined visually and confirmed morphologically by inspecting the shrimp’s branchial chambers. Female-male pairs of Pr. pandalicola were easily discernible under the carapace and confirmed in a small subset of shrimp using a dissecting microscope (Fig. 3A–D). The length of each shrimp was measured from the tip of the rostrum to the end of the uropods to the nearest 0.1 mm following protocols from Kirkham et al. (2021), and their width was measured below the gills at the first pereomere. Parasite length and width were also measured to the nearest millimeter using calipers by measuring the anterior margin of the head to the end of the pleotelson, and width was measured at the first pereomere. Female parasites were measured exclusively; parasite males were not measured because of their small size. Wet weight was recorded for all shrimp and bopyrid isopods to the nearest 0.001 g.

Figure 3.

Photographs taken using a dissecting microscope during parasite processing showing (A) Daggerblade grass shrimp, Paleomon pugio, parasitized by ecotoparasite Probopyrus pandalicola (B) daggerblade grass shrimp, with the male-female bopyrid isopod pair Pr. pandalicola in the shrimp branchial chamber (C) daggerblade grass shrimp with an ovigerous Pr. pandalicola in its branchial chamber, and (D) a close-up image of the ovigerous Pr. pandalicola in the shrimp branchial chamber. Color version available online.

Figure 3.

Photographs taken using a dissecting microscope during parasite processing showing (A) Daggerblade grass shrimp, Paleomon pugio, parasitized by ecotoparasite Probopyrus pandalicola (B) daggerblade grass shrimp, with the male-female bopyrid isopod pair Pr. pandalicola in the shrimp branchial chamber (C) daggerblade grass shrimp with an ovigerous Pr. pandalicola in its branchial chamber, and (D) a close-up image of the ovigerous Pr. pandalicola in the shrimp branchial chamber. Color version available online.

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Data analysis

We used the ‘lmer4’ package (Bates et al., 2015) to construct a quasibinomial model to explore which parameters best explained the variation of Pr. pandalicola prevalence in infected shrimp. This model included salinity, shrimp density, and panne distance from shore as predictor variables. All statistical analyses were conducted using R v.4.20 (R Core Team, 2022). Similar to Johnson (2014), we evaluated near-surface ocean temperature data from 2016 to 2020 from Cape Cod, Massachusetts, and compared to it water temperature from 2021 (US National Data Buoy Center, Station 44018) to evaluate temperature-related drivers of Pr. pandalicola prevalence.

Total Pr. pandalicola prevalence across Cape Cod in August 2021

Five marsh sites across Cape Cod were sampled in August 2021 (Fig. 1). We collected 2,263 grass shrimp in total, 220 of which were parasitized by Pr. pandalicola (9.7% prevalence). Shrimp infested with Pr. pandalicola had a single female parasite or male-female parasite pair present in 1 branchial chamber and no cases of infestation of both branchial chambers. Prevalence varied between salt marshes and was far higher in Cummaquid, with 14.1% (213 of 1,515) of the grass shrimp infested. All other salt marshes had <5% Pr. pandalicola prevalence with the distribution as follows: Sandwich (1% parasite prevalence), Wellfleet (0.35% parasite prevalence), Yarmouth Port (4.1% parasite prevalence), and Dennis (0% parasite prevalence).

Pr. pandalicola prevalence in Cummaquid

Across all seasons (summer, fall, and spring), 12.8% of the 2,665 grass shrimp collected across 13 pannes in Cummaquid were infested with Pr. pandalicola (n = 342). Shrimp were most abundant during the warmer months of the summer (n = 1,515 shrimp, mean temperature: 25.6 C), followed by fall (n = 741 shrimp, mean temperature: 16 C), and spring (n = 409 shrimp, mean temperature: 8.3 C; Fig. 2B). Every panne sampled in summer had shrimp infestation present, while 6 of 7 pannes sampled in fall and 3 of 7 pannes sampled in spring had shrimp infestation present. Overall, the highest prevalence of Pr. pandalicola was in spring (median ± standard deviation 21% ± 4.87%, n = 70 infected shrimp), followed by summer (15% ± 9.66%, n = 213 infected shrimp), then fall (6% ± 4.06%, n = 59 infected shrimp; Fig. 2B). Although the actual number of infected shrimp was variable, the highest prevalence of Pr. pandalicola infestation was recorded at individual pannes 6 (30.3%, n = 36 infected shrimp) and 9 (25.9%, n = 25 infected shrimp) in summer (Fig. 2C). All parasites were found on both male and female shrimp in male-female pairs, and summer was the only time in which ovigerous female Pr. pandalicola were present. There was a significant positive relationship between grass shrimp abundance and Pr. pandalicola abundance (parasite vs. shrimp counts, n = 9, adjusted R2 = 0.35, P = 0.05; Fig. 4A), driven by the high abundance of Pr. pandalicola (n = 70) and grass shrimp (n = 324) observed in panne 12 (Fig. 5A). Measurements on all grass shrimp and Pr. pandalicola collected from Cummaquid across seasons and pannes revealed significant positive relationships between shrimp length (6–42 mm) and female parasite length (<1–8 mm) (n = 338, adjusted R2 = 0.47, P < 0.001; Fig. 5A) and shrimp wet weight (0.4–60 mg) and parasite length (n = 338, adjusted R2 = 0.45, P < 0.001; Fig. 5B).

Figure 4.

(A) Relationship between shrimp count and parasite count from pannes. (B) Relationship between the prevalence of parasites from pannes to the distance to shore.

Figure 4.

(A) Relationship between shrimp count and parasite count from pannes. (B) Relationship between the prevalence of parasites from pannes to the distance to shore.

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Figure 5.

(A) Relationship between parasite length and shrimp length from pannes. (B) Relationship between parasite length and shrimp carapace width from pannes.

Figure 5.

(A) Relationship between parasite length and shrimp length from pannes. (B) Relationship between parasite length and shrimp carapace width from pannes.

Close modal

Probopyrus pandalicola prevalence increased with panne distance from the marsh edge (n = 9, adjusted R2 = 0.43, P = 0.05; Fig. 4B). Panne area, shrimp counts, and panne distance from the edge of the marsh all significantly correlated with parasite prevalence (Table I). Salinity varied widely across pannes in Cummaquid across all seasons (5–35 ppt) and was not correlated with grass shrimp infestations in Cummaquid in August. Based on year-over-year averages, the water temperature from Cape Cod in 2021 was 0.68 C higher (13 C) than yearly averages from 2016 to 2020 (12.3 C).

Table I.

Results from the quasibinomial model comparing parasite prevalence on grass shrimp (Paleomon pugio) in Cummaquid pannes to panne area, shrimp count, and panne distance to shore. Statistically significant relationships (P < 0.05) are in bold.

Results from the quasibinomial model comparing parasite prevalence on grass shrimp (Paleomon pugio) in Cummaquid pannes to panne area, shrimp count, and panne distance to shore. Statistically significant relationships (P < 0.05) are in bold.
Results from the quasibinomial model comparing parasite prevalence on grass shrimp (Paleomon pugio) in Cummaquid pannes to panne area, shrimp count, and panne distance to shore. Statistically significant relationships (P < 0.05) are in bold.

This research documented the prevalence of the bopyrid isopod (Pr. pandalicola) in an abundant and ecologically influential host species (grass shrimp) in salt marsh habitats of New England. Our results describe a relatively high prevalence of bopyrid parasitism of grass shrimp in Cape Cod, Massachusetts. Although in extreme cases Pr. pandalicola have been reported to infest up to 25% of a grass shrimp population, it is typical for them to infest <1% of grass shrimp in many locations, and in general, studies report low prevalence of infestations by bopyrid isopods on carideans (Heard and Lutz, 1982; Sheehan et al., 2011; Briggs et al., 2017; Finn and Buck, 2024). Here the prevalence of Pr. pandalicola in grass shrimp was higher than other published reports (for instance, 12.8% infestation across 3 seasons in Cummaquid and a single panne yielding a 30.3% infestation in summer; Table II), although bopyrid prevalence in grass shrimp in the present study was comparable to other species of grass shrimp (17.7% of a population of Palaemon ritteri were parasitized in Baja, California; Campos and Campos, 1989), and generally lower than brown shrimp hosts (up to 34% of Crangon spp were parasitized in Humboldt Bay, California; Jay, 1989). Although the high prevalence of Pr. pandalicola is noteworthy, this study also provides the first documentation of Pr. pandalicola in this region in almost 75 years (the last documentation of Pr. pandalicola in New England was from 1950). This suggests a lack of observations of this species in New England, which to our knowledge have not been reported on in the literature in more than 70 years.

Table II.

Comparison of Palaemon pugio parasitized by Probopyrus pandalicola throughout the literature, shown as total prevalence.

Comparison of Palaemon pugio parasitized by Probopyrus pandalicola throughout the literature, shown as total prevalence.
Comparison of Palaemon pugio parasitized by Probopyrus pandalicola throughout the literature, shown as total prevalence.

In this study we describe the presence, and high prevalence, of a host-parasite association poorly described in its northern range. The seasonal and geographic context of host-parasite relationships is important to note as we attempt to quantify climate-driven changes. For example, in marine systems, shifts in water characteristics (i.e., temperature, salinity, oxygen, nutrients) can influence host susceptibility, parasite intensity, and pathology, which may impact host-parasite relationships, while large-scale climate shifts may alter the range of their occurrence (Byers, 2021). Furthermore, shifts in host-parasite relationships have the potential to influence salt marsh community dynamics. Here we explore relationships between parasite prevalence in grass shrimp and spatial/environmental parameters, which indicate the combination of panne area, shrimp abundance, and distance from the marsh edge all contribute to the high parasite prevalence measured in this study.

Bopyrid parasite abundance and size were correlated with grass shrimp abundance and size in this study (Figs. 4, 5). Similar relationships between definitive shrimp host size and bopyrid infestation have been observed in several other systems, although it should be mentioned that these studies determined shrimp size differently from our study, ranging from measuring shrimp carapace length (CL; Smith et al., 2008) to total length (TL; Bortolini Rosales et al., 2021, to total length converted to CL (Whalen et al., 2020). Nonetheless, mature, reproductively viable grass shrimp are more likely to be infested by bopyrids than young shrimp. Taken together, these findings suggest that on a small scale, the high prevalence of shrimp infestation on mature individuals, and subsequent sexual sterilization of shrimp (also called “reproductive death”; Calado et al., 2008), may influence shrimp mortality and, ultimately, population dynamics. For instance, in one study evaluating the effects of bopyrid isopods and parasitic trematodes on grass shrimp, shrimp had decreased survivorship over the course of the experiment compared to uninfected shrimp, although no significant difference was seen in shrimp mortality infected with bopyrid isopods or a parasitic trematode (Finn and Buck, 2024).

Similarly, the parasitic isopod Tachaea chinensis has been found to infect the shrimp Palaemonetes sinensis in rice fields of Lianing Province, China, leading to shrimp mortality (Li et al., 2018). Population declines have been observed with mud shrimp (Upogebia pugettensis) infested with the bopyrid isopod (Orthione griffenis) in the Pacific Northwest, although it should be noted that this species of bopyrid is non-native, likely exerting stronger controls on shrimp populations as there has not been co-evolution between parasite and host (Dumbauld et al., 2011). Additionally, grass shrimp have high site fidelity, residing in individual pools within a salt marsh or intertidal creek basin (Allen et al., 2015). Thus, once parasites are present, localized shrimp infestation and sterilization may become much higher.

Alternatively, some literature indicates that bopyrid isopods may not drive non-predative host mortality of grass shrimp, as the survival of the isopod is dependent on the survivorship of the shrimp (Finn and Buck, 2024). Bopyrid isopods appear to decrease the risk of their hosts being predated, possibly through shifts in shrimp behavior (Bass and Weis 1999; Brinton and Curran, 2015a; Finn and Buck, 2024). Additionally, there are systems in which the prevalence of parasitic castrators is high, and yet host populations are not particularly affected because hosts have co-evolved with their parasites. For example, trematode prevalence in California horn snails can be >90%, but the parasites do not measurably influence recruitment because the hosts have evolved a high reproductive output as compensation (Buck et al., 2017). Further work investigating host-parasite relationships is required to properly evaluate how parasite prevalence will impact shrimp populations over time.

Grass shrimp directly influence the processing of detrital material and meiofauna abundances, and as such, a high prevalence of parasitism in a relatively confined panne environment may also indirectly influence other levels of biological organization. The loss of grass shrimp as key detritivores and abundant food source may negatively affect salt marsh community and ecosystem dynamics, where high parasite prevalence at individual pannes, and female shrimp sterilization, would result in the loss of these species processing organic matter (also suggested by Brinton and Curran, 2015b). Similarly, altered behavior exhibited by infected grass shrimp may influence predator-prey dynamics, and thus ecological communities within salt marshes. For instance, parasitized grass shrimp have been found to exhibit decreased backward thrusting in the presence of a predator, mummichogs (Fundulus heteroclitus) while also making hosts more conspicuous to predators (visually the parasites diminish shrimp camouflage; Brinton and Curran, 2015a). It is important to note that although we explored the relationship between Pr. pandalicola parasite prevalence and grass shrimp size, we did not examine the possible relationship between the sex of grass shrimp and the developmental stage of the bopyrid parasite. Documenting parasite developmental stage alongside host size would provide specific host-parasite associations, such as indicating if parasitized male hosts are larger than unparasitized hosts or non-ovigerous parasitized female hosts. These interactions are necessary to explore, as they may influence the population structure of the host grass shrimp population.

Many potential mechanisms may be driving the high prevalence of Pr. pandalicola infestation in grass shrimp, and although in this study we were ultimately unable to identify drivers of Pr. pandalicola prevalence, we sought to describe possible relationships between key abiotic factors and parasite presence. Dagglerblade grass shrimp are euryhaline and tolerant to a range of salinities (<1–30 ppt; Heard and Lutz, 1982); however, salinity tolerance of Pr. pandalicola remains largely undocumented. Initial reports of Pr. pandalicola prevalence in grass shrimp in the southern United States describe higher parasite prevalence with higher salinities and temperatures, although habitat type and land use were confounding factors (Key et al., 2011; Briggs et al., 2017). In Hartnoll (1982), temperature was found to have a stronger influence on crustaceans (in the intermolt stage) with minimal effects by salinity. In Cummaquid, Massachusetts, there was no apparent relationship between salinity and grass shrimp abundance or parasite abundance. Although no strong relationship was seen between salinity and parasites, Bass and Weiss (1999) found that parasitized grass shrimp showed significantly reduced activity levels at higher salinities (15 ppt and 26 ppt) than unparasitized shrimp, suggesting that salinity may be an important driver of infected grass shrimp behavior, rather than Pr. pandalicola prevalence itself. Further research is needed to investigate how salinity may influence grass shrimp behavior because possible consequences hold for trophic dynamics between predators of infected grass shrimp in situ. For instance, increased predation on slower infected grass shrimp in salty water may lead to lower densities of grass shrimp and, as such, reflect higher densities of parasitized grass shrimp in less salty water.

The configuration of the pannes in Cummaquid also appeared to influence both grass shrimp and parasite prevalence, irrespective of salinity or any other abiotic factor. For instance, some pannes were farther inland in the high marsh, which likely had less tidal flushing than pannes that were closer to shore (thus retaining more grass shrimp and their parasites). This was observed as an increase in both parasites and shrimp with increasing distance from the shoreline, with no apparent difference in salinity associated with distance to the shoreline. Aquatic vegetation present within pannes facilitating habitat for grass shrimp and their parasites, in addition to other habitat characteristics (e.g., panne topography and/or flushing), could be drivers of Pr. pandalicola prevalence. As such, further research is required to establish the full extent to which abiotic factors (e.g., temperature and salinity) as well as biotic factors, including the larval transport and abundance of the intermediate copepod hosts of Pr. Pandalicola, drive parasite prevalence (Sasaski et al., 2023). For instance, dos Santos Periera et al. (2022) suggest that bopyrid parasites in certain regions of Brazil are limited by the distribution of estuarine copepods. To this end, it is necessary to disentangle drivers of parasite distribution from potentially confounding factors (i.e., panne placement within a marsh).

In 2021 we observed an increased abundance of grass shrimp in the warmer months of the summer and fall, and Pr. pandalicola was also abundant in the warmer summer months, although it is notable that Pr. pandalicola had the highest prevalence in the spring. Although it is unclear why parasites were most prevalent in cooler spring temperatures, it is not surprising that Pr. pandalicola were exclusively ovigerous in the summer when grass shrimp have been found to molt, thus continuing the parasitic life cycle (Brinton and Curran, 2015b). Warming ocean temperatures may play an important role in influencing host-parasite interactions and thus shrimp survivorship. For instance, Sherman and Curran (2013) found decreased survivorship of grass shrimp that were parasitized by Pr. pandalicola in warmer water (25 ± 0.10 C) than uninfected shrimp. In this study, temperatures on Cape Cod, Massachusetts, in 2021 were warmer compared to previous years (2016–2020), and so future work should consider the relationship between water temperature and Pr. pandalicola prevalence and define possible temperature-driven shifts in grass shrimp and Pr. pandalicola populations.

In temperate coastal marshes of the United States, the loss of total salt marsh area combined with the transient nature of salt pannes is resulting in shifts in salt marsh populations, with cascading effects on salt marsh communities and ecosystem dynamics. In this study the high prevalence of parasites on daggerblade grass shrimp, a key species in salt marshes, may result in important shifts in all levels of biological organization. Specifically, we must have a preliminary understanding of the distribution of Pr. pandalicola, as they may play a role in structuring grass shrimp populations in salt marsh ecosystems. Further, the ranges of host species and the ranges and prevalence of parasites may be shifting as climate change intensifies and associated abiotic characteristics shift. Since changes in the range and distribution of many species are known to have meaningful impacts on ecosystem structure, functioning, and stability, understanding the prevalence and range of parasites and their hosts is essential.

The authors wish to thank A. Boyd for sample guidance and processing, R. Jenkins, B. Powers, A. Granzier, and L. West for sample processing, I. Ives and M. Faherty for logistical guidance and support, and the Massachusetts Audubon Long Pasture Wildlife Sanctuary for the use of their land and facilities. Comments by S. Archer and 2 anonymous reviewers greatly improved the manuscript.

Allen,
D. M.,
Harding
J. M.,
Stroud
K. B.,
and
Yozzo
K. L.
2015
.
Movements and site fidelity of grass shrimp (Palaemonetes pugio and P. vulgaris) in salt marsh intertidal creeks
.
Marine Biology
162
:
1275
1285
. .
Anderson,
G.
1975
.
Metabolic response of the caridean shrimp Palaemonetes pugio to infection by the adult epibranchial isopod parasite Probopyrus pandalicola
.
Comparative Biochemistry and Physiology Part A: Physiology
52
:
201
207
. .
Anderson,
G.
1977
.
The effects of parasitism on energy flow through laboratory shrimp populations
.
Marine Biology
42
:
239
251
. .
Anderson,
G.
1985
.
Species profiles: Life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico)—Grass shrimp
.
U.S. Fish and Wildlife Service Biological Report 82(11.35)
.
U.S. Army Corps of Engineers, TR EL-82-4
,
19
p.
Baeza,
J. A.,
Steedman
S.,
Prakash
S.,
Liu
X.,
Bortolini
J. L.,
Dickson
M.,
and
Behringer
D. C.
2018
.
Mating system and reproductive performance in the isopod Parabopyrella lata, a parasitic castrator of the ‘peppermint’ shrimp Lysmata boggessi
.
Marine Biology
165
:
41
. .
Bass,
C. S.,
and
Weiss
J. S.
1999
.
Behavioral changes in the grass shrimp, Palaemonetes pugio (Holthuis), induced by the parasitic isopod, Probopyrus pandalicola (Packard)
.
Journal of Experimental Marine Biology and Ecology
241
:
223
233
. .
Bates,
D.,
Mächler
M.,
Bolker
B.,
and
Walker
S.
2015
.
Fitting linear mixed-effects models Usinglme4
.
Journal of Statistical Software
67
:
1
48
. .
Beck,
J. T.
1979
.
Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea)
.
Parasitology
79
:
431
449
. .
Bortolini Rosales,
J. L.,
Mejía Estrada
J. A.,
Alonso Reyes
M. D. P.,
Romero Rodríguez
J.,
and
Baeza
J. A.
2021
.
Reproductive biology of the bopyrid isopod Robinione overstreeti, a branchial parasite of the ghost shrimp Callichirus islagrande (Decapoda: Callichiridae) in the Gulf of Mexico
.
Marine Biology Research
17
:
247
259
. .
Briggs,
S. A.,
Blanar
C. A.,
Robblee
M. B.,
Boyko
C. B.,
and
Hirons
A. C.
2017
.
Host abundance, seagrass cover, and temperature predict infection prevalences of parasitic isopods (Bopyridae) on Caridean shrimp
.
Journal of Parasitology
103
:
653
662
. .
Brinton,
B. A.,
and
Curran
M. C.
2015a
.
The effects of the parasite Probopyrus pandalicola (Packard, 1879) (Isopoda, Bopyridae) on the behavior, transparent camouflage, and predators of Palaemonetes pugio Holthuis, 1949 (Decapoda, Palaemonidae)
.
Crustaceana
88
:
1265
1281
. .
Brinton,
B. A.,
and
Curran
M. C.
2015b
.
The effect of temperature on synchronization of brood development of the Bopyrid Isopod parasite Probopyrus pandalicola with molting of its host, the Daggerblade Grass Shrimp Palaemonetes pugio
.
Journal of Parasitology
101
:
398
404
. .
Buck,
J. C.,
Hechinger
R. F.,
Wood
A. C.,
Stewart
T. E.,
Kuris
A. M.,
and
Lafferty
K. D.
2017
.
Host density increases parasite recruitment but decreases host risk in a snail–trematode system
.
Ecology
98
:
2029
2038
. .
Byers,
J. E.
2021
.
Marine parasites and disease in the era of global climate change
.
Annual Review of Marine Science
13
:
397
420
.
Calado,
R.,
Bartilotti
C.,
Goy
J.,
and
Dinis
M.
2008
.
Parasitic castration of the stenopodid shrimp Stenopus hispidus (Decapoda: Stenopodidae) induced by the bopyrid isopod Argeiopsis inhacae (Isopoda: Bopyridae)
.
Journal of the Marine Biological Association of the United Kingdom
88
:
307
309
. .
Campos,
E.,
and
Campos
A. R.
1989
.
Epicarideos de Baja California: Distribución y notas ecológicas de Probopyrus pandalicola (Packard, 1879) en el Pacifico oriental
.
Journal of Tropical Biology
37
:
29
35
. .
Cash,
C. E.,
and
Bauer
R. T.
1993
.
Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae)
.
Journal of Crustacean Biology
13
:
111
124
. .
Chaplin-Ebanks,
S. A.,
and
Curran
M. C.
2007
.
Prevalence of the bopyrid isopod Probopyrus pandalicola in the grass shrimp, Palaemonetes pugio, in four tidal creeks on the South Carolina-Georgia coast
.
Journal of Parasitology
93
:
73
77
. .
Collins
H.
Jr.,
1981
.
Harper & Row’s Complete Field Guide to North American Wildlife: Eastern Edition
.
Harper & Row Publishers
,
New York, New York, 1
,
523
p.
De Grave,
S.,
and
Ashelby
C. W.
2013
.
A re-appraisal of the systematic status of selected genera in Palaemoninae (Crustacea: Decapoda: Palaemonidae)
.
Zootaxa
3734
:
331
344
. .
Dobson,
A.,
Lafferty
K. D.,
Kuris
A. M.,
Hechinger
R. F.,
and
Jetz
W.
2008
.
Colloquium paper: Homage to Linnaeus: How many parasites? How many hosts
?
Proceedings of the National Academy of Sciences of the United States of America
105
(
Suppl 1
):
11482
11489
. .
dos Santos Pereira,
R. I.,
Maciel
C. R.,
and
Iketani
G.
2022
.
Molecular features of Probopyrus sp. (Isopoda: Bopyridae) from Brazilian Amazonia and the parasitism of inland populations of Macrobrachium amazonicum (Decapoda: Palaemonidae)
.
Parasitology
149
:
203
208
. .
Dumbauld,
B. R.,
Chapman
J. W.,
Torchin
M. E.,
and
Kuris
A. M.
2011
.
Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific Coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)
?
Estuaries and Coasts
34
:
336
350
. .
Finn,
R. P.,
and
Buck
J. C.
2024
.
Opposing life history strategies allow grass shrimp parasites to avoid a conflict of interest
.
Oecologia
204
:
365
376
. .
Fowler,
H. W.
1912
.
The Crustacea of New Jersey, Annual Report of the New Jersey State Museum 1911 (Part II)
.
New Jersey State Museum
,
Trenton, New Jersey
, p.
29
650
.
Hammerschlag-Peyer,
C. M.,
Allgeier
J. E.,
and
Layman
C. A.
2013
.
Predator effects on faunal community composition in shallow seagrass beds of the Bahamas
.
Journal of Experimental Marine Biology and Ecology
446
:
282
290
. .
Hartnoll,
R. G.
1982
. Growth. In
The Biology of Crustacea, 2, Embryology, Morphology and Genetics
,
Bliss
D. E.
and
Abele
G.
(eds.).
Academic Press
,
New York, New York
, p.
111
196
.
Hatcher,
M. J.,
and
Dunn
A. M.
2011
.
Parasites in Ecological Communities: From Interactions to Ecosystems
.
Cambridge University Press
,
Cambridge, UK
,
445
p.
Heard,
R. W.,
and
Lutz
L. B.
1982
.
Guide to Common Tidal Marsh Invertebrate Prevalences of the Northeastern Gulf of Mexico
.
Alabama Sea Grant Consortium
. Available at:
EZID
: https://repository.library.noaa.gov/view/noaa/13648. Accessed 11 June 2023.
Jay,
C. V.
1989
.
Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum
.
American Midland Naturalist
121
:
68
77
.
Johnson,
D. S.
2014
.
Fiddler on the roof: A northern range extension for the marsh fiddler crab Uca pugnax
.
Journal of Crustacean Biology
34
:
671
673
. .
Key,
P.,
West
B. J.,
Pennington
P. L.,
Daugomah
J. W.,
and
Fulton
M.
2011
. Effects of land use and physicochemical water quality on grass shrimp, Palaemonetes pugio, and its parasitic isopod, Probopyrus pandalicola, in
South Carolina, USA tidal creeks. NOAA Technical Memorandum NOS NCCOS 125
.
NOAA/National Centers for Coastal Ocean Science
,
Charleston, South Carolina
,
28
p.
Kirkham,
J. S.,
Guidone
M.,
and
Curran
M. C.
2021
.
Spatial and temporal trends in parasite infections of the daggerblade grass shrimp Palaemon pugio in coastal Georgia
.
Estuarine, Coastal and Shelf Science
260
:
107508
. .
Kunkel,
B. W.
1918
.
The Arthrostraca of Connecticut
.
Bulletin of the State Geological and Natural History Survey of Connecticut
26
:
1
261
.
Lafferty,
K. D.,
Dobson
A. P.,
and
Kuris
A. M.
2006
.
Parasites dominate food web links
.
Proceedings of the National Academy of Sciences of the United States of America
103
:
11211
11216
. .
Leonardos,
I.,
and
Trilles
J.-P.
2003
.
Host-parasite relationships: Occurrence and effect of the parasitic isopod Mothocya epimerica on sand smelt Atherina boyeri in the Mesolongi and Etolikon Lagoons (W. Greece)
.
Diseases of Aquatic Organisms
54
:
243
251
.
Li,
Y.,
Xu
W.,
Li
X.,
Jiang
H.,
She
Q.,
Han
Z.,
Li
X.,
and
Chen
Q.
2018
.
Comparative transcriptome analysis of Chinese grass shrimp (Palaemonetes sinensis) infected with isopod parasite Tachaea chinensis
.
Fish and Shellfish Immunology
82
:
153
161
.
Ludwig,
K. D.
2009
.
The effects of coded wire tags and the isopod parasite Probopyrus pandalicola on the growth and predation of Daggerblade grass shrimp Palaemonetes pugio Holthuis (1949)
.
M.S. Thesis
.
Savannah State University
,
Savannah, Georgia
,
125
p.
Manderson,
J. P.,
Phelan
B. A.,
Stoner
A. W.,
and
Hilbert
J.
2000
.
Predator–prey relations between age-1+ summer flounder (Paralichthys dentatus, Linnaeus) and age-0 winter flounder (Pseudopleuronectes americanus, Walbaum): Predator diets, prey selection, and effects of sediments and macrophytes
.
Journal of Experimental Marine Biology and Ecology
251
:
17
39
. .
Markham,
J. C.
1985
.
A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico
.
Memoirs of the Hourglass Cruises
7
:
1
156
.
McCall,
D. D.,
and
Rakocinski
C. H.
2007
.
Grass shrimp (Palaemonetes spp.) play a pivotal trophic role in enhancing Ruppia maritima
.
Ecology
88
:
618
624
. .
Morris,
J. A.
1948
.
Studies on the host-parasite relationship of Probopyrus pandalicola (Packard)
.
Biological Studies, Catholic University of America
8
:
1
20
.
Morton,
J. P.,
and
Silliman
B. R.
2020
.
Parasites enhance resistance to drought in a coastal ecosystem
.
Ecology
101
:
e02897
. .
Packard,
A. S.
1879
.
Zoology for Students and General Readers
.
Henry Holt & Co
.,
New York, New York
,
719
p.
Pennings,
S. C.,
and
Bertness
M. D.
2001
. Salt marsh communities. In
Marine Community Ecology
,
Bertness
M. D.,
Gaines
S. D.,
and
Hay
M.
(eds.).
Sinauer Associates
,
Sunderland, Massachusetts
, p.
289
316
.
R Core Team
.
2022
.
R: A language and environment for statistical computing
.
R Foundation for Statistical Computing
,
Vienna, Austria
.
Ribeiro,
F. B.,
Horch
A. P.,
and
Williams
J. D.
2019
.
New occurrences and host records for two species of parasitic isopods (Isopoda, Cymothoida, Bopyridae) associated with caridean shrimps (Decapoda, Caridea) from Brazil
.
Journal of Natural History
53
:
2437
2447
. .
Richardson,
H.
1904
.
Contributions to the natural history of the Isopoda
.
Proceedings of the United States National Museum
27
:
1
89
.
Richardson,
H.
1905
.
Monograph on the isopods of North America
.
Bulletin of the United States National Museum
54
:
1
727
.
Roche,
D. G.,
Strong
L. E.,
and
Binning
S. A.
2013
.
Prevalence of the parasitic cymothoid isopod Anilocra nemipterid on its fish host at Lizard Island, Great Barrier Reef
.
Australian Journal of Zoology
60
:
330
333
. .
Sasaski,
M.,
Woods
C.,
and
Dam
H. G.
2023
.
Parasitism does not reduce thermal limits in the intermediate host of a bopyrid isopod
.
Journal of Thermal Biology
117
:
103712
. .
Sheehan,
K. L.,
Lafferty
K. D.,
O’Brien
J.,
and
Cebrian
J.
2011
.
Parasite distribution, prevalence, and assemblages of the grass shrimp, Palaemonetes pugio, in Southwestern Alabama, U.S.A
.
Comparative Parasitology
78
:
245
256
. .
Sherman,
M. B.,
and
Curran
M. C.
2013
.
The effect of the bopyrid isopod Probopyrus pandalicola (Packard, 1879) (Isopoda, Bopyridae) on the survival time of the daggerblade grass shrimp Palaemonetes pugio Holthuis, 1949 (Decapoda, Palaemonidae) during starvation at two different temperatures
.
Crustaceana
86
:
1328
1342
. .
Sherman,
M. B.,
and
Curran
M.C.
2015
.
Sexual sterilization of the Daggerblade grass shrimp Palaemonetes pugio (Decapoda: Palaemonidae) by the bopyrid isopod Probopyrus pandalicola (Isopoda: Bopyridae)
.
Journal of Parasitology
101
:
1
5
. .
Sikora,
W. B.
1977
.
The ecology of Palaemonetes pugio in a southeastern salt marsh ecosystem with particular emphasis on production and trophic relationships
.
Ph.D. Dissertation
.
University of South Carolina
,
Columbia, South Carolina
,
122
p.
Smith,
A. E.,
Chapman
J. W.,
and
Dumbauld
B. R.
2008
.
Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia Pugettensis
.
Journal of Crustacean Biology
28
:
228
233
. .
Smithsonian National Museum of National History
.
Invertebrate Zoology Collection. Catalog No
.
USNM
91223
. Available at: https://collections.nmnh.si.edu/search/iz/?ark=ark:/65665/3c421ed59cb7f4e398283a181c7d47f82. Accessed 14 September 2023.
Smithsonian National Museum of National History
.
Invertebrate Zoology Collection. Catalog No
.
USNM
91224
. Available at: https://collections.nmnh.si.edu/search/iz/?ark=ark:/65665/30cdd8fa7c42e4468b6c850d4835fb7a8. Accessed 14 September 2023.
Smithsonian National Museum of National History
.
Invertebrate Zoology Collection. Catalog No
.
USNM
91225
. Available at: https://collections.nmnh.si.edu/search/iz/?ark=ark:/65665/36c79f80419574cfa864874ea52e14c02. Accessed 14 September 2023.
Smithsonian National Museum of National History
.
Invertebrate Zoology Collection. Catalog No
.
USNM
39428
. Available at: https://collections.nmnh.si.edu/search/iz/?ark=ark:/65665/3c175126f931b4a40b032b3d58e01ffb7. Accessed 14 September 2023.
Sumner,
F. B.,
Osburn
R. C.,
and
Cole
L. J.
1913
.
A biological survey of the waters of Woods Hole and vicinity
.
Section I. Physical and zoological. Bulletin of the Bureau of Fisheries, U.S. Fish and Wildlife Service
31
:
1
441
.
US (DOC/NOAA/NWS/NDBC) National Data Buoy Center
.
1971
.
Meteorological and oceanographic data collected from the National Data Buoy Center Coastal-Marine Automated Network (C-MAN) and moored (weather) buoys. [Nantucket Sound Station ID: 44020, temperature]
.
NOAA National Centers for Environmental Information
.
Dataset. Available at: https://www.ncei.noaa.gov/archive/accession/NDBC-CMANW. Accessed 29 September 2022
.
Welicky,
R. L.,
and
Sikkel
P. C.
2014
.
Variation in occurrence of the fish-parasitic cymothoid isopod, Anilocra haemulid, infecting French grunt (Haemulon flavolineatum) in the north-eastern Caribbean
.
Marine and Freshwater Research
65
:
1018
1026
. .
Welsh,
B. L.
1975
.
The role of Grass Shrimp, Palaemonetes Pugio, in a tidal marsh ecosystem
.
Ecology
56
:
513
530
. .
Whalen,
M. A.,
Millard-Martin
B. R.,
Cox
K. D.,
Lemay
M. A.,
and
Paulay
G.
2020
.
Poleward range expansion of invasive bopyrid isopod, Orthione griffenis Markham, 2004, confirmed by establishment in Central British Columbia, Canada
.
Bioinvasions Records
9
:
538
548
. .
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