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Ecology and epidemiology of the striped shrimp, Pandalus montagui Leach, 1814 (Decapoda: Caridea), in the northern

Labrador Sea, Davis Strait, and Ungava Bay, Canada

Krista D. Baker1, , David A. Fifield2, , Darrell R.J. Mullowney1 and Katherine R. Skanes1,

1Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St. John’s, Newfoundland and Labrador, A1C 5X1, Canada; and2Environment and Climate Change Canada, Wildlife Research Division, Mount Pearl, Newfoundland and Labrador, A1N 4T3, Canada

Correspondence: K. Baker; e-mail: Krista.Baker@dfo-mpo.gc.ca

(Received 11 March 2021; accepted 3 May 2021)

ABSTRACT

Despite a fishery with annual landings valued at over $50 million CAD, very little knowledge has been gathered about the ecology of the striped shrimp (Pandalus montagui Leach 1814) in the Canadian northwestern Atlantic. This information is nevertheless considered essential for developing appropriate management actions for the fishery. We used survey data collected from 2005 to 2020 in the northern Labrador Sea, Ungava Bay, and Davis Strait to examine sizes, stages of maturity, size of transition, and evidence of parasites in the striped shrimp. We also investigated potential ecological drivers affecting the presence of parasites and size of transition. We found shrimp were substantially larger than previously observed in nearby habitats. The size of transition did not remain constant throughout the time series, and in-stead, was a function of the average size of females and the amount of preferred habitat in the previous year. The probabilities of individuals exhibiting black gill or black shell disease, or being infected with a bopyrid parasite were generally related to sex, depth, temperature, salinity, latitude, and shrimp density. The large sizes observed in the study area and the ap-parent plasticity of the population to environmental changes indicate that this species should be closely monitored in the future in relation to exploitation pressure and climate change.

Key Words: fisheries, maturity, northwestern Atlantic, pandalid shrimps, shrimp diseases, shrimp parasites, size of transition

INTRODUCTION

The striped shrimp (Pandalus montagui Leach 1814) is primarily considered bycatch in the larger northern shrimp (P.  borealis Krøyer 1838) fishery in the Labrador Sea and Davis Strait, eastern Canada, with only occasional reports of targeted fishing activities. Striped shrimp, however, is the primary species targeted in Ungava Bay, eastern Canada. During the last decade the striped shrimp fishery in eastern Canada has landed between 4,228 metric tonnes (t) and 11,374 t annually, and had an estimated landed value of approximately $57 million CAD in 2019 (Fisheries and Oceans Canada, unpublished data).

The eastern Canadian shrimp fishery mainly occurs during ice-free conditions in three management units termed “shrimp fishing areas” (SFAs): Western Assessment Zone (WAZ), Eastern Assessment Zone (EAZ), and SFA 4 (Fig. 1). The Pandalus spp.

fishing industry consists of factory freezer trawlers (> 33 m (100 ft) vessel sector), as well as smaller inshore trawlers (Fisheries and Oceans Canada, 2018). Both sectors primarily use bottom otter trawls with a minimum mesh size of 40  mm, and mandatory sorting mechanisms in the trawls, termed Nordmore grates, to minimize bycatch (Fisheries and Oceans Canada, 2018). There is no minimum legal size for the striped shrimp, but the netting is thought to exclude most individuals smaller than 17.5 mm cara-pace length (CL) (Labonté & Fréchette, 1978).

The striped shrimp is found from Davis Strait, Canada to Rhode Island, USA, northwestern Atlantic (Squires, 1996). Unlike P. borealis, the striped shrimp is regularly found in relatively shallow waters (< 180 m) throughout most of its range (Squires, 1996). Striped shrimp are protandrous hermaphrodites, changing sex from male to female throughout their lives. In northern parts of

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Journal of Crustacean Biology Advance Access published 24 June 2021

Journal of

Crustacean BiologyJournal of Crustacean Biology (2021) 41(2), 1–11. doi:10.1093/jcbiol/ruab024

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their range, most (if not all) individuals develop into mature males early in their lives, then transition to females at approximately 17 mm CL, conforming to ages three or four years (Squires, 1996; Bergström, 2000). In the northeastern Atlantic, transitions from male to female stages begin in February, but occur throughout the summer months (Simpson et al., 1967). In the northwestern Atlantic off Newfoundland and Labrador, ovigerous females are found throughout the year, but most prevalent from July to September (Squires, 1996). Spawning occurs in the late fall to early winter in the northeastern Atlantic and hatching occurs from March to April (Mistakidis, 1957; Allen, 1959, 1963; Bergström, 2000). Females lay a single batch of eggs annually (Allen, 1963), but likely release eggs at least twice in their lifespan and live to approximately six years of age (Squires, 1996).

Despite an active Pandalus spp. fishery since the late 1980s, the lack of consistent scientific surveys in the northern Labrador Sea, Davis Strait, and Ungava Bay meant that the fishery was gener-ally being managed with little regionally based knowledge of the ecology of the species. In response a collaborative survey between industry and Fisheries and Oceans Canada (DFO) was initiated, in 2005 to provide information regarding the population status and ecology of shrimp stocks in these northern areas.

We present the first comprehensive study of striped shrimp based on data collected from 2005 to 2020 in the northern Labrador Sea, Davis Strait, and Ungava Bay. We describe striped shrimp habitat characteristics, stages of maturity, size of transi-tion, and epidemiology (e.g., evidence of a suite of diseases and infections), as well as investigate potential ecological drivers of epi-demiological infections and size of transition.

MATERIALS AND METHODS

Survey data

The Northern Shrimp Research Foundation (NSRF) survey is a collaborative survey between NSRF and DFO used to assess the abundance and health of shrimp (Pandalus spp.) populations off northern Labrador and Baffin Island, Nunavut (Siferd, 2015). The survey occurs during the summer (late June to August) using a modified Campelen 1800 shrimp trawl. The trawl has 0.53 m rockhopper footgear, a vertical opening of about 3.96 m, a wing spread of approximately 16.84 m, and a cod-end liner of 12.5 mm mesh (Walsh & McCallum, 1997). The survey follows a random-stratified statistical design, with strata based on depth and stations randomly assigned within each stratum, and the number of sta-tions allocated proportional to the area of each stratum. For each tow, the vessel aims to travel at 3.0 knots with 15 min of bottom contact. Bottom temperature, salinity, and depth are recorded during each tow using a trawl-mounted CTD (conductivity, tem-perature, and depth). The average of all CTD measurements taken from the start to the end of the tow is considered the swept-area value for that tow (Siferd, 2015). Catchability (capture effi-ciency) for the striped shrimp is assumed to be 1 for individuals encountered by the trawl.

A subsample of shrimps caught during each tow were sorted to species and then characterized based on maturity, presence of parasites, shell condition, and carapace length (Siferd, 2015). Maturity categories included male, transitional, ovigerous female, primiparous female, and multiparous female. Primiparous and multiparous females were distinguished based on the presence (primiparous) or loss (multiparous) of sternal spines (McCrary, 1971). Primiparous and multiparous females were further divided into individuals with head roe (ovaries with mature oocytes) and those without it. Overall condition assessments represented shell condition (hard or soft) along with the screening for the presence of epidemiological diseases or pathogens: black gill disease (the ciliate Synophyra sp.), parasitism by a bopyrid isopod (Hemiarthrus abdominalis (Krøyer, 1840)), black shell (pathogen unknown), and a microsporidian (Microsporidium spp.). The shrimp in each category were weighed to the nearest 0.01  g (Siferd, 2015). The oblique carapace length (base of eye to posterior edge of carapace) of each individual in the subsample was measured with digital cali-pers to the nearest 0.01 mm (Siferd, 2015). The weights and num-bers of shrimp in each tow were standardized to a 0.8 nm tow.

Data were collected annually in SFA 4 and EAZ from 2005 to 2020, but there was incomplete survey coverage in EAZ in 2005 and 2006. In WAZ, the survey was conducted annually from 2014 to 2020. Length frequency data from WAZ in 2014 were unavailable. To account for these inconsistencies within the time series, all trend analyses were completed at the SFA level and using a restricted data set (SFA 4 entire time series, EAZ 2007–2020, WAZ 2015–2020).

Data analyses

Standardization of male catches. Since male striped shrimp have been documented moving off the bottom and into the water column during the night (Hudon et al., 1992), their capture probability is reduced, and night tows are likely to lead to an underestimate of true population abundance by the survey. To identify the effect

Figure 1. Set locations of the Northern Shrimp Research Foundation collaborative survey. Size of points represent standardized number (1,000s) of striped shrimp (Pandalus montagui) in a tow (Shrimp Fishing Area, SFA 4: 2005–2020, Eastern Assessment Zone, EAZ: 2007–2020, Western Assessment Zone, WAZ: 2014–2020.

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of period on survey catches, a generalized additive model (GAM) that related catch to temperature, salinity, stratum, year, and period was implemented using the mgcv package (Wood, 2017) in R 4.0.2 (R Core Team, 2020). Period was classified as night or day based on light categories recorded during each tow. Dark, moonlight, and dusk and dawn were classified as night, while dull-overcast, bright but hazy, and bright sunlight were classified as day. Depth was not included in the model since it was collinear with temperature and had a variance inflation factor (VIF) greater than 3 (Zuur et al., 2010). We tested for interaction between period and temperature, salinity, and stratum and found no significant inter-active effects. The best fitting model was a GAM, with a Gamma family (log link) distribution:

Eq. 1:

Yi ∼ Gamma (ui, r)

E (Yi) = ui, var (Yi) =u2i �r

log (ui) = βo + periodi + yeari + stratumi

+ f1 (temperaturei) + f2 (salinityi)

where, Yiis the standardized number of males in a tow, β o is the intercept, period is factor taking values “night” or “day,” year is a factor representing the year the survey took place, stratum is a factor indicating the stratum where the tow occurred, the fi’s are unique smooth functions of the given covariates and calculated for each year: temperature is the bottom temperature (°C) recorded during the tow, and salinity is the salinity recorded during the tow. The smooth functions were computed with thin-plate regression splines with a maximum basis dimension of 10.

The coefficient of period from the fitted model was used to con-vert catches of males during night tows, thereby standardizing all catches to the daylight period.

Size and maturities. The stages of maturity were examined within each SFA through time using the annual proportion of each stage within 0.5 mm CL bins. The data were searched for females less than 10  mm CL as possible evidence of early-maturing or pri-mary females. The range and average size of males, transitionals, primiparous, and multiparous females were identified.

The annual size of transition was estimated as the carapace length at which 50% of the population had transitioned (L50). Following Pedersen (2018), L50 was calculated for each combin-ation of SFA and year using a GAM with a binomial distribution.

Eq. 2:

Yi ∼ binomial (1, pi)

E (Yi) = pivar (Yi) = pi × (1− pi)

logit (pi) = βo + fj (CLi) + SFA_yeari

where, Yi represents transitioned (i.e., transitional or female) or not yet transitioned (i.e., male) for an individual of a given cara-pace length (mm) in a given SFA and year, β o is the intercept, and fj is a unique smooth function of carapace length estimated using a thin-plate smoothing spline for each SFA/year combination (SFA_yeari). Each observation was weighted by the number of in-dividuals sampled in the set of that particular transitional-size cat-egory. L50 was estimated for each SFA and year by determining the length at which the model fitted value was 0 (on the logit scale), which corresponds to 50% probability of transition (since logit(0) = e0/(1 + e0) = 50% probability) (see Pedersen, 2018).

Various potential predictors of trend in the annual L50 in each SFA were examined. Potential predictors considered included

average habitat index based on temperature (SFA specific and for the three SFAs combined), female biomass, male biomass, ratio of male to female biomass, average female size (SFA-specific and for the three SFAs combined), and exploitation rate indices (all pre-dictors were lagged by one year). Annual biomass and exploitation rate indices were obtained from stock assessments for each SFA (K.R. Skanes et  al., unpublished data, W.  Walkusz et  al., unpub-lished data). Monthly bottom temperatures from 2004 to 2019 were obtained from the Bedford Institute of Oceanography North Atlantic Model (BNAM, Wang et al., 2018). The habitat index was estimated from the average annual area (km2) with bottom tem-peratures between –0.3 and 2.7 °C (based on unpublished analysis of striped shrimp’s preferred temperature range in the study area). The best fitting model was a GAM, with a Gamma family (log link) distribution.

Eq. 3:

L50i ∼ Gamma (ui, r)

E (L50i) = ui, var (L50i) = u2i �r

log (ui) = βo + SFAi + f1 (F_CLi) + f2 (HIi)

where, L50iis the annual estimated carapace length (mm) when 50% of the individuals have started transition within each SFA, β o is the intercept, SFAi is a factor representing the shrimp fishing area, the fi’s are smooth functions of the given covariates: F_CLi is the average carapace length (mm) of females in the previous year within the three SFAs combined, and HIi is the average habitat index for the three SFAs combined in the previous year. The smooth functions were computed with thin-plate regression splines with a maximum basis dimension of 8.

Epidemiology. The annual trends in the prevalence of striped shrimp observed with black gill disease, bopyrid isopod parasitism, black shell, and a microsporidian (%) were examined. GAMMs (gen-eralized additive mixed models) with binomial distributions were used to identify significant predictors of the conditions, except for a microsporidian infection where the prevalence was low and sporadic (see results). Eq. 4 represents the model considered for each condition.

Eq. 4:

Yi ∼ binomial (ni, pi)

E (Yi) = pi × nivar (Yi) = ni × pi × (1− pi)

logit (pi) = βo + f1 (tempi) + f2 (sali) + f3 (depthi)

+ f4 (densityi) + f5 (latitudei) + sexi + γi

where, Yiis the standardized number of striped shrimp of a particular sex with the condition in a tow, ni is the total number of striped shrimp of a sex in a given standardized tow, β o is the intercept, the fi’s are smooth functions of the given covariates: temp is bottom temperature (°C) recorded during the tow, sal is salinity (psu) recorded during the tow, depth is depth (m) of the tow, density is the total number of striped shrimp in the tow (to in-vestigate density dependence), sex is either male, female, or transi-tional, and γi is a random intercept for each combination of SFA and year. The smooth functions were computed with thin-plate re-gression splines with a maximum basis dimension of 5.

RESULTS

A total of 4,332 trawl sets were completed between 2005 and 2020 (Fig. 1). Depths of tows ranged from 100 m to 742 m, bottom temperatures from –1.7 to 12 °C, and salinities from 31.2

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psu to 34.94 psu. Striped shrimp were caught in 1,775 of these sets, and over 154,440 individuals were measured and sampled (Fig. 2). Striped shrimp were found in waters with bottom temper-atures between –1.6 and 4.7 °C, depths between 100 and 686 m, and salinities throughout the full range of salinities sampled by the survey (31.2 to 34.9 psu) (Table 1, Fig. 3).

Standardization of night-time male catches

The model for identifying the effect of period on male catch rates indicated that daylight catches were 1.52 times those made at night (P < 0.001). Accordingly, this conversion factor was applied to all subsequent analyses (54.1% deviance explained).

Size and maturities

Striped shrimp sampled ranged in size from 6 to 32.5  mm CL, with the average size of males 17.2  mm, primiparous females 21.5 mm, and multiparous females 22.4 mm (Table 2). Only one female less than 10 mm CL was sampled in the 16 years of data, meaning that early-maturing females were virtually absent from our survey area at the time of sampling. Transitionals sampled during the survey ranged in size from 10 to 28 mm (Table 2).

Modelled L50 (66.7% deviance explained) declined from 2005 to 2014 in SFA 4.  This was followed by an increase until 2020, when it was above 20  mm (Fig. 4). L50 in EAZ varied through time, but EAZ consistently had larger L50 estimates than those recorded in both SFA 4 and WAZ. The time series for WAZ was too short to identify a trend, but L50 peaked in 2019 within the short timeframe.

The annual modelled L50 trends within each SFA were a func-tion of large-scale stock dynamics and processes, with the average carapace length of females within all SFAs in the previous year

(P = 0.001) and the habitat index within all SFAs in the previous year (P  <  0.001) being significant predictors in the model (67% deviance explained). As the habitat index and size of females in the previous year increased, the L50 also increased (Fig. 5). SFA 4 had significantly smaller L50s than EAZ (P < 0.001). The L50s in WAZ were also smaller than those estimated in EAZ, but the dif-ference was only weakly significant (P = 0.041).

A large proportion of the females in EAZ and WAZ were cat-egorized as ovigerous, whereas females could be identified as a mix of primiparous and multiparous with a smaller portion of ovigerous in SFA4 (Fig. 6). A small proportion of the catches have been transitionals in all areas since 2009. Relatively small-sized transitional and primiparous females were identified in SFA 4 in 2018 and 2019.

Figure 2. Number of striped shrimp (Pandalus montagui) sampled within each shrimp fishing area (SFA) from 2005 to 2020 during the Northern Shrimp Research Foundation collaborative survey.

Table 1. Ranges of temperature, salinity, and depths where the striped shrimp (Pandalus montagui) was found during the Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020).

Temperature (°C) Salinity (psu) Depth (m)

EAZ –1.6–4.6 31.2–34.9 129–686

SFA 4 –1.5–4.7 32.5–34.9 116–535

WAZ –1.3–3.3 32.1–34.4 100–674

Figure 3. The standardized number of striped shrimp (Pandalus montagui) in a tow based on bottom temperature, bottom salinity, and depths from the Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2005–2020, WAZ: 2014–2020).

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Epidemiological conditions

Almost all striped shrimp with evidence of any of the epidemio-logical conditions (i.e., black gill, black shell, microsporidian, or bopyrid isopod) showed evidence of one condition. The per-centage of the catch with a single condition peaked in EAZ in 2019 at over 10% and in SFA 4 in 2013 at more than 9%, whereas during the last six years the overall prevalence of any conditions remained below 0.7% in WAZ. When two epidemiological con-ditions were found, they were black shell and the presence of a bopyrid isopod (EAZ: 2012, 2013, and SFA 4: 2008) or black shell and a microsporidian (EAZ: 2009).

The prevalence of black gill was low throughout all SFAs, with an overall mean of 0.31% and many years having no evidence of the condition in the survey (Fig. 7, Table 3). A notable exception was in EAZ during 2019, when the prevalence of black gill peaked at nearly 10%. Although much lower prevalence was observed in SFA 4 and WAZ, the prevalence of black gill in each of these areas also peaked in 2019. The prevalence of black shell condi-tions was relatively high in both SFA 4 and EAZ, with a time-series average of 3.53% and 2.40%, respectively, and reaching a high of 9.64% in 2012 in EAZ. In both areas, the prevalence of black shell has been at the lowest values in the time series during the last five years. The infection rates of a bopyrid isopod were relatively high during the beginning of the time series in SFA 4, but appear low during the last three years of the survey. Isopod infections are below 0.25% in almost all years in EAZ and par-ticularly low during the last three years. In contrast, 2020 repre-sented the highest prevalence of isopods in WAZ. Microsporidian infections were rare, with no clear trend in prevalence through the time series. Average values for all areas were 0.02%, with a peak of 0.16% in SFA 4 in 2019.

Given the trends and overall prevalence, the occurrence of striped shrimp with isopod infections, black shell, and black gill in each standardized tow was modelled in an attempt to identify

potential predictors of their presence. Modelling efforts found that the odds of finding a striped shrimp with the isopod was a func-tion of sex, temperature (P  <  0.001), salinity (P  <  0.001), depth (P  <  0.001), density (P  <  0.001), and latitude (P  <  0.001) (4.2% deviance explained, Fig. 8). Male striped shrimp were 5.1× more likely to be infected with the parasite than females (P < 0.001), but transitionals were not significantly more likely to be infected than females (P = 0.51). The occurrence of the isopod increased with increasing salinity and generally declines with increasing tem-perature. The partial effects of depth, latitude, and density are variable.

The likelihood of a striped shrimp having black shell was a func-tion of numerous variables including sex, temperature (P < 0.001), salinity (P  <  0.001), depth (P  <  0.001), density (P  <  0.001), and latitude (P  <  0.001) (60.5% deviance explained, Fig. 8). Female striped shrimp are 2.1× more likely to have black shell than males (P < 0.001), and 1.8× more likely than transitionals (P < 0.001). There appears the possibility of a strong density dependence, where the likelihood of having black shell is increased as density increases. The strong decline at the tail end of the density logit-effects plot should be examined with skepticism as it represents the model attempting to fit to only four data points beyond 70,000, three of which had no black shell recorded and the other had 0.09% of the population with black shell. In general, the partial effect of latitude becomes more negative with increasing latitude. It appears as though the greatest positive effects of temperature and salinity are in the tail ends of the environments sampled. The effect of depth becomes positive in waters deeper than approxi-mately 500 m.

The overall likelihood of a striped shrimp having black gill is ex-tremely small. The model found that likelihood to be significantly influenced by sex, temperature (P  <  0.001), salinity (P  <  0.001), depth (P  <  0.001), density (P  <  0.001), and latitude (P  <  0.001) (81.7% deviance explained, Fig. 8). Males were 3.9× more likely to have black gill than females (P < 0.001) and females were 2.3× more likely to have black gill than transitionals (P < 0.001). The partial effects of temperature were negative below approximately –0.4  °C and above 2.5  °C. The likelihood of a striped shrimp being documented with black gill is highest at the shallowest and deepest areas of the survey area and the edges of the survey area farthest north and south.

DISCUSSION

Habitat generalizations

Temperature, salinity, and substrate are considered the major factors determining the distribution of Pandalus spp. (Bergström, 2000). The general habitat characteristics identified in our sur-veys generally correspond well with previous reported habitat descriptions. Although the striped shrimp has a wide tempera-ture tolerance from –1 to over 20 °C in the northeastern Atlantic (Bergström, 2000), Squires (1996) reported shrimp in bottom tem-peratures of –1.0 to 0.5 °C in the northwestern Atlantic. In con-trast, we found individuals in waters colder than –1 °C and in a

Table 2. Summary of carapace lengths (mm) of striped shrimp (Pandalus montagui) measured during the Northern Shrimp Research Foundation collabora-tive survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020).

Area Male Transitional Primiparous females Multiparous females

Mean Range Mean Range Mean Range Mean Range

SFA 4 16.7 6.0–26.5 21.4 10.0–28.0 21.2 12.0–28.0 22.6 8.0–30.5

EAZ 17.4 8.0–27.5 22.0 16.0–26.5 21.9 17.0–29.0 22.4 15.0–32.5

WAZ 17.7 7.5–30.5 20.6 15.5–25.0 21.2 16.5–28.5 22.0 16.5–29.0

Total 17.2 21.5 21.5 22.4

Figure 4. Annual model-predicted carapace length (mm) of striped shrimp (Pandalus montagui) at 50% transition in each shrimp fishing area (SFA). The lines (and shaded 95% confidence intervals) represent a loess regression fit to the annual points. The model is based on Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020).

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wider temperature range than those reported by Squires (1996), with positive catches in waters ranging from –1.6 to 4.7  °C. Shrimp have been reported in waters up to 10 °C (Wigley, 1960) off New England, USA. Although relatively warm waters (> 5 °C) were sampled, no shrimp were recorded in these areas.

The wide temperature tolerance of the striped shrimp is one factor that is thought to have allowed populations to inhabit a var-iety of depths, including shallow waters (Bergström, 2000). We found shrimp in the shallowest depths surveyed (~100 m), but did not record any individuals deeper than 686 m. Squires (1996) reported shrimp in waters 90 to 320 m, and Bergström (2000) noted that the shrimp is most commonly caught in waters 20 to 100 m. Given the general correlation of cold water and shallow areas in our study area, it may be necessary to extend the survey into shallower waters to better understand the full dynamics of this stock.

In respect of salinity, Bergström (2000) noted that striped shrimp were found in waters with salinity values ranging from ap-proximately 25 to 35 psu. We found individuals in waters up to 35 psu.

Although we did not directly address substrate, our findings would appear to align with the habitat substrate description pro-vided by Bergström (2000), who described that striped shrimp are found on a variety of bottom types, but to show a tendency to prefer hard bottoms. This conforms with the high densities in shallow waters, which generally correspond with hard substrates in our study area (Piper, 1991).

Night-time male catches

Our observations correspond with previous reports of males moving up in the water column during the night to feed (e.g., Hudon et al., 1992). Crawford et al. (1992) found that some striped shrimp undertook nocturnal vertical migrations (sometimes over 200 m off the bottom) following zooplankton near Resolution Island (which is within our study area) during autumn months. The diel migrations began when light intensity began to diminish (Crawford et al., 1992; Hudon et al., 1992). Stomach analyses indi-cated that these vertical migrations corresponded with planktonic, pelagic feeding (Hudon et al., 1992). It has been hypothesized that ovigerous P.  borealis females may not migrate vertically because eggs attached to their pleopods reduce their swimming ability (Bergström, 2000). Hudon et  al., (1992) found ovigerous striped shrimp in the water column but attributed those relatively rare oc-currences to passive drift as a result of turbulence.

No estimates of the effect of diel period on striped shrimp catches could be found in the literature, but Fréchette et al., (1983) found P.  borealis to be 1.9 to 6.33 times more abundant in day

catches than in night survey tows. Although our estimate of 1.52 for the shrimp is less than those published for P. borealis, our sur-veys occur in summer Arctic conditions, where the effect of the midnight sun and minimal darkness may dampen the overall diel migration pattern.

Size and maturities

The largest striped shrimp observed in the northwestern Atlantic from 1957 to 1960 was 28 mm (Squires, 1996), whereas the lar-gest individuals sampled during our survey were substantially larger (32.5 mm CL) and even the largest male observed in each SFA was near or above 28 mm. Similarly, size of transitional in-dividuals recorded in our surveys indicated much larger sizes than those reported for striped shrimp off Newfoundland and Labrador and Quebec. Squires (1996) and Couture & Trudel (1969) re-ported transitionals ranging from 17 to near 20  mm CLs. The transitional shrimp measured during our surveys had average CLs above 20 mm.

Simpson et al., (1967) reported striped shrimp having an average life expectancy of three to four years, with individuals aged four to five years between 16 and 19  mm CLs in the northeastern Atlantic. The average time a shrimp remains a male may in-crease with an increasing life span (Charnov, 1982). Northerly populations of pandalid shrimps grow more slowly, have longer life spans, and reach larger sizes than more southerly popula-tions (Bergström, 2000). Since our data were collected near the northern limit of the species distribution in the northwestern Atlantic, it would be expected that the overall size and size of transition may be somewhat larger than samples taken farther south. The magnitude of difference observed between historical reports and those in our surveys is nevertheless large and striking. The estimated ages corresponding to maturity phases and life span should be re-examined in the survey area in light of the not-able larger sizes recorded.

Based on the mesh size used in the commercial fishery, the fishable size of pandalid shrimps is considered > 17.5 mm CL. This size was thought to allow most shrimp to transition to fe-males before becoming targeted by the fishery. The large size of males and transitionals reported within the survey indicate that this is likely not an effective strategy for protecting repro-ductive potential of the population, with many transitioning at sizes much larger than the fishable size. Striped shrimp are therefore likely more vulnerable to exploitation than previously considered.

Although the overall transitional sizes sampled in our survey are larger than those reported elsewhere, the decade-long, slow, and gradual decline of size of transition in SFA 4 in the sampled

Figure 5. Response-scale partial effects of average female carapace length (mm) and habitat index (km2) on the annual carapace length (mm) at 50% tran-sition for striped shrimp (Pandalus montagui). The values on the y-axis correspond to the additive effect on annual carapace length at 50% transition for given values of the x-axis covariate in the model. The model is based on data from Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020).

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data is notable. Since female length is a function of size of tran-sition and female fecundity is proportional to approximately cube of body length, the egg production would decline as the length of transition becomes smaller (Shumway et al., 1985; Wieland, 2004). Even seemingly small changes in L50 of the population over time

could have large effects on the fecundity and reproductive poten-tial of the population.

The sudden occurrence of small-size (<15 mm CL) transitional individuals observed in SFA 4 in 2019 were notable. These values more closely resemble the sizes (10 to 20 mm CL) of transitional

Figure 6. The proportion of striped shrimp (Pandalus montagui) during the Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020) classified as male, or transitional, primiparous, multiparous or ovigerous females by size in each year by shrimp fishing area (SFA).

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striped shrimp recorded in the northwestern Atlantic by Squires (1996). There were 13 occurrences of these small transitional in-dividuals and all but one was from two sets in a single stratum. There were no signs of parasites or disease that might have caused this relatively early transitioning.

Pandalid shrimps are able to alter their age and size of transi-tion in response to annual fluctuations in their environment and population demographics (Charnov & Anderson, 1989). In other species of Pandalus, the prevalence and timing of sexual transitions

have been linked to a variety of potential factors including lati-tudinal distribution, genetics (Bergström, 2000), temperature (Wieland, 2004), fishing mortality (Charnov, 1982), and popu-lation density (Koeller et  al., 2000). For example, P.  borealis ad-just their size of transition in relation to the size of other nearby breeding adults; when the breeders in the population are large, the transition size is large (Charnov & Anderson, 1989).

Our results indicate that striped shrimp may be responding similarly in relation to the size of nearby females, whereby L50

Figure 7. The prevalence (%) of striped shrimp (Pandalus montagui) with black gill, black shell, or infections with a bopyrid isopod, or a microsporidian during the Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020).

Table 3. The prevalence (%) of pathogens and conditions in striped shrimp (Pandalus montagui) during the Northern Shrimp Research Foundation collab-orative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020). Max., maximum values.

Area Black gill Black shell Bopyrid isopod Microsporidian

Mean Max. Mean Max. Mean Max. Mean Max.

SFA 4 0.05 0.38 3.53 9.06 0.34 0.95 0.04 0.16

EAZ 0.73 9.95 2.40 9.64 0.13 0.32 0.01 0.04

WAZ 0.02 0.09 0.26 0.49 0.13 0.27 0.01 0.03

Total 0.31 2.55 0.22 0.02

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increases in response to larger females in the population. Since large females are more fecund than small females, this response may be a result of maximizing reproductive fitness (Bergström, 2000). The significant positive relationship of L50 with the habitat index indicates that as more thermal habitat is available, male striped shrimp grow to larger sizes before transitioning to female.

Noteworthy, we did not find significant relationships between the annual L50 estimates and exploitation rates, female biomass, or male biomass, as has been noted in other pandalid shrimps (e.g., Charnov & Bergström, 1987; Hannah & Jones, 1991).

Although early-maturing striped shrimp females are found in other populations, they are rarely or never found in Arctic waters

Figure 8. Logit-scale partial effects of significant predictors of the likelihood of that a striped shrimp (Pandalus montagui) will be infected with a bopyrid isopod (Hemiarthrus abdominalis) or with black gill (Synophrya sp.), or exhibit black shell condition. The models are based on data from Northern Shrimp Research Foundation collaborative survey (SFA 4: 2005–2020, EAZ: 2007–2020, WAZ: 2015–2020). The tail end of the density plots represents the models attempting to fit to only four data points with values greater than 70,000 shrimp.

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(Shumway et  al., 1985; Bergström, 2000). The lack of particu-larly early-maturing or primary females in 16  years of surveys supports the hypothesis that small females are virtually absent in northerly waters.

Under current sampling techniques, ovigerous females cannot be categorized as primiparous or multiparous because the eggs block view of the sternal spines used to differentiate these categories. The ability to distinguish primiparous and multip-arous females in SFA 4, but not WAZ and EAZ, is likely a result of timing of the survey within each area. The survey in SFA 4 was completed before EAZ and WAZ. In SFA 4, the survey can begin as early as late June, with the majority of the sets occurring in mid-July. In comparison, WAZ and EAZ surveys generally end near early August, but can extend into late August. Previous re-ports from Newfoundland and Labrador have noted that a lower proportion of females were ovigerous in May and June, compared to July to September, when the proportion of females in the popu-lation that were ovigerous peaked (Squires, 1996). Our data focus on an area farther north, where the passing of eggs from the head (non-ovigerous) to the abdomen (ovigerous) may be somewhat de-layed in comparison (at least in SFA 4). This phenomenon and the slight difference in survey timing may be causing the difference in proportions of females with different maturities found in the SFAs.

Epidemiology of parasitic infections

Black gill is caused by Synophrya sp., an apostome ciliate found in the gill lamellae feeding on the hemolymph of Pandalus spp. (Orr et  al., 2011; Lee et  al., 2019). No estimates of its prevalence in striped shrimp populations could be found in the literature, but it is considered the most prevalent parasite of P.  borealis off Newfoundland and Labrador (Orr et al., 2011), with estimates of 0.5 and 14% between 2001 and 2009. Prevalence has been noted as high as 80% in P. borealis in the Gulf of Maine, where it is con-sidered to be at epidemic levels (Lee et al., 2019). By comparison, the prevalence of black gill in striped shrimp in our survey was relatively low (usually less than 1%) and sporadic. Nevertheless, the recent peaks of infections in all areas highlight the need to continue to monitor this parasite and gain more knowledge about its potential impact on the population.

Shrimps parasitized by a microsporidian give the appearance of being cooked, with the musculature of the abdomen, ceph-alothorax, pleopods, and pereiopods becoming whitish opaque (Olson & Lannan, 1984; Parsons & Khan, 1986). Infections can occur in both sexes and transitional stages (Parsons & Khan, 1986). Infected male P.  borealis may have poorly developed vasa deferentia and infected females have poorly developed ovaries, reducing (or eliminating) their mating capacity (Parsons & Khan, 1986). Parsons & Khan (1986) also found low prevalence (0.04%) of a microsporidian infection in P. borealis off Labrador from 1981 to 1984. Pandalus jordani Rathbun, 1902 infections off Oregon from 1975 to 1980 were also found to be very low proportion (0.19%). The time-series average of infections in striped shrimp for our entire survey area was lower than those noted in P.  borealis off Labrador, with little to no indication of the parasite in some years and sporadic peaks of infection rates, particularly in SFA 4.

The average annual prevalence of the bopyrid isopod H. abdominalis in our surveys is similar to other documented occur-rences in striped shrimp populations. Hemiarthrus abdominalis have been identified infecting striped shrimp off Greenland, Norway, and Britain, but with low prevalence in all locations (Allen, 1966; Simpson et  al., 1967). Prevalence of H.  abdominalis in striped shrimp in a North Sea estuary averaged monthly values of near 0.47%, with a peaked frequency at only 3.9% (Warren, 1974), much higher than the highest prevalence noted in the 16  years of our survey. There are no known seasonal fluctuations in the prevalence of H. abdominalis in the striped shrimp populations re-searched (Warren, 1974). The documented prevalence of parasitic

infections of bopyrid isopods in P.  borealis is also generally low; infection in the Barents Sea averaged 0.23% in 1978 and 1979 (Teigsmark, 1983), less than 2% off Greenland (Horsted & Smidt, 1956), and no infection detected off Northumberland, United Kingdom (Allen, 1959).

Our findings are consistent with the literature showing that H.  abdominalis is more prevalent in male Pandalus spp. Infection with bopyrid isopods lead to changes in sexual characteristics in males. Teigsmark (1983) found that infected male P.  borealis had transitional endopodite characteristics, and female striped shrimp infected with H.  abdominalis carried 50% less eggs (Mistakidis, 1957). In striped shrimp, H.  abdominalis have been documented to greatly reduce the number of eggs that attach successfully and develop normally (Allen, 1966). Although the prevalence of this parasite has remained low during our time series, the recent peaks in SFA 4 and WAZ highlight that more research into the impact of this parasite on reproductive health of this population may be warranted.

Black shell is a generic condition related to a striped shrimp’s response to repairing shell damage. The source of the damage is unspecified. It was the most observed condition during our sur-veys, but the repercussions of black shell in striped shrimp and the ultimate causes remain unknown.

The prevalence of all the conditions examined were signifi-cantly related to environmental conditions, such as temperature and salinity. The ultimate causal effect of these predictors on the vulnerability of striped shrimp and/or the abundance of the para-site remains unknown.

Currently, as a bycatch species, the characteristics of striped shrimp in northern Labrador Sea, Ungava Bay, and Davis Strait (e.g., presence of parasites, and size of transition) are significantly influenced by environmental conditions. The combination of slow growth rates, large sizes, plasticity of the population, and fishable size nevertheless would indicate that close examination of this resource in relation to exploitation pressure and climate change should remain a priority.

ACKNOWLEDGEMENTS

Wojciech Walkusz and Sheila Atchison provided survey-data files from DFO-Arctic Region and provided insight into the intricacies of the data. Dr. Zeliang Wang kindly provided BNAM data. Julia Pantin, William Coffey, and Brittany Beauchamp provided DFO-internal reviews of the manuscript prior to submission. The NSRF collaborative survey could not be completed without the dedica-tion and hard work of many industry and Indigenous partners. The manuscript was improved by helpful suggestions from two an-onymous reviewers and the Associate Editor.

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