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Does the bopyrid parasite Probopyrus pandalicola affect the predation
preferences of mummichogs by altering the behavior and/or camouflage
of the grass shrimp Palaemonetes pugio?
Brigette A. Brinton and Mary Carla Curran
Department of Marine and Environmental Sciences, Savannah State University
The bopyrid isopod Probopyrus pandalicola is a hematophagous ectoparasite that infects palaemonid shrimp, including the daggerblade
grass shrimp Palaemonetes pugio. Isopod parasites affect shrimp physiology and possibly behavior, but may also decrease the transparent
camouflage of their grass shrimp hosts. The purpose of this study was to determine if Probopyrus pandalicola affected the predation
preferences of a visual predator, the mummichog Fundulus heteroclitus, by altering the behavior and/or camouflage of its grass shrimp
prey. The effects of the parasite were differentiated by camouflage and/or behavior by pairing combinations of parasitized,
unparasitized, and marked shrimp. The branchiostegite of marked shrimp was painted to mimic the appearance of the parasite. Two
shrimp were presented to two mummichog predators in 23x13x16 cm aquaria (n=106). Mummichog preference and shrimp behavior
immediately prior to a predation event were recorded. Both the behavioral and visual effects of the parasite affected predator preference.
Parasitized shrimp swam more (P=0.048) and backward thrusted less (P=0.027) than unparasitized shrimp immediately prior to
predation. Across all shrimp pairings, mummichogs preferentially selected the more active shrimp (83/84 replicates), and selected the
less camouflaged shrimp if there was no difference in shrimp behavior (19/22 replicates). Parasitized shrimp were preferentially
consumed (51/85 shrimp) if they were paired with unparasitized shrimp, as they behaved differently and were more poorly
camouflaged than unparasitized shrimp. Although the sample size was small, marked shrimp were not preferentially selected over
unparasitized shrimp (8 and 4 shrimp, respectively), nor were parasitized shrimp preferentially selected over marked shrimp (6 and 2
shrimp, respectively). The major findings of this study were that Probopyrus pandalicola affected the predation preferences of
mummichogs through changing both shrimp behavior and camouflage. Ultimately, a possible benefit of parasitization may be a decrease
in a high visibility behavior such as backward thrusting, thereby impacting predator-prey dynamics in estuarine ecosystems.
Abstract
Introduction
The physical appearance of Probopyrus pandalicola and/or its
potential effect on the behavior of its host Palaemonetes pugio
affects the predation preferences of Fundulus heteroclitus
Hypothesis
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 52(A):201-207.
Anderson, G. and W.E. Dale. 1981. Probopyrus pandalicola (Packard) (Isopoda, Epicaridea): morphology and development of larvae in culture.
Crustaceana 41(2):143-161.
Bass, C.S. and J.S Weis. 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(1999):223-233.
Bakker, T.C.M., D. Mazzi, and S. Zala. 1997. Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology,
78 (4):1098-1104.
Bhandiwad, A. and S. Johnsen. 2011. The effects of salinity and temperature on the transparency of the grass shrimp Palaemonetes pugio. Journal of
Experimental Biology 214: 709-716.
Chaplin-Ebanks, S.A. and M.C. Curran. 2005. The effect of the parasitic isopod, Probopyrus pandalicola (Packard, 1879), on tidal activity patterns of the
grass shrimp, Palaemonetes pugio Holthuis, 1949. Crustaceana 78(9):1053-1061.
Clark, K.L., G.M. Ruiz, and A.H. Hines. 2003. Diel variation in predator abundance, predation risk, and prey distribution in shallow-water estuarine
habitats. Journal of Experimental Marine Biology and Ecology 287:37-55.
Kensley, B., and M. Schotte. 1989. Guide to the marine isopod crustaceans of the Caribbean. Smithsonian Institution Press. Washington, D.C. 273 p.
Kunz, A.K., M. Ford, and O.J. Pung. 2006. Behavior of the grass shrimp Palaemonetes pugio and its response to the presence of the predatory fish Fundulus
heteroclitus. American Midland Naturalist 155(2):286-294.
Morgan, S.G. 1987. Morphological and behavioral antipredatory adaptations of decapod zoeae. Oecologia 73(3):393-400.
Sherman, M.B., and M.C. Curran. 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 (11): 1328-1342.
Smith, G.M. and J.S. Weis. 1997. Predator-prey relationships in mummichogs (Fundulus heteroclitus (L.)): Effects of living in a polluted environment.
Journal of Experimental Marine Biology and Ecology 209:75-87.
Welsh, B.L. 1975. The role of grass shrimp, Palaemonetes pugio, in a tidal marsh ecosystem. Ecology 56(3):513-530.
Williamson, C.J., P.L. Pennington, and M.C. Curran. 2009. Toxicity of synthetic pyrethroid insecticides to the grass shrimp, Palaemonetes pugio, parasitized
with the bopyrid isopod, Probopyrus pandalicola. Journal of Environmental Science and Health Part B 44: 810-816.
Literature Cited
Funding was provided by NSF GK-12 Award # DGE-0841372, Savannah State University and the
NOAA Living Marine Resources Cooperative Science Center Award # NA17AE1626.
Drs. Sue Ebanks and Dionne Hoskins provided valuable feedback on this research. Additional
editing and collection assistance was provided by many students and technicians at Savannah
State University, particularly Michele Sherman, Cameron Brinton, and Kate Doyle.
Acknowledgments
Materials and Methods
Three types of shrimp were used in order from most to least
camouflaged: unparasitized shrimp, parasitized shrimp, and
unparasitized shrimp that were marked with paint so that they
resembled parasitized shrimp (Pictured above).
Shrimp were paired in order to differentiate between the effects of the
parasite on shrimp behavior and/or camouflage (Table 1).
Each 2.5 L aquarium replicate (n=106) contained 2 fish and 2 shrimp
(Figure 2). The difference in total length within each pair was ≤ 5%;
shrimp length was ≤ 40% of fish length. The difference in trematode
intensity (metacercarial cysts per shrimp) within each pair of
shrimp was restricted to ≤ 5.
Fundulus heteroclitus and Palaemonetes pugio were starved for 24 h prior
to each trial. All trials were conducted during the daytime and
during ebb tide because of the known effects of these variables on
shrimp behavior as noted by Chaplin-Ebanks and Curran (2005).
The behavior of both shrimp was recorded just prior to predation by F.
heteroclitus. Organisms were observed for a maximum of 30 min.
Mummichogs consumed the more active shrimp across all
shrimp pairings (78.3% of all shrimp), and selected the less
camouflaged shrimp 19/22 times (17.9% of all shrimp)
(p=0.0017) if there was no difference in shrimp behavior
(Figure 3). Parasitized shrimp were preferentially consumed
(51/85) if they were paired with unparasitized shrimp
(p=0.0096) (Table 1). Mummichogs tended to consume
marked shrimp over unparasitized shrimp as well, but the
sample size was low (Table 1).
Predator preference was affected by shrimp behavior (p<0.0001).
Mummichogs consumed backward-thrusting shrimp most
frequently (69.2%), while motionless shrimp were consumed
least often (0.3%) (Figure 4). Furthermore, 100% of parasitized
shrimp that backward thrusted were consumed, while 18.5%
of the unparasitized shrimp that backward thrusted did
successfully avoid predation.
Shrimp behavior immediately prior to predation was affected by
the parasite (p=0.036). Parasitized shrimp swam more (37.6%)
(p=0.048) and backward thrusted less (15.3%) (p=0.027) than
unparasitized shrimp (21.2% and 31.8%, respectively).
Results
Discussion
The major finding of this study was that Probopyrus pandalicola
affected the behavior and camouflage of its host as well as the
predation preferences of Fundulus heteroclitus.
Parasitized shrimp backward thrusted less frequently, and therefore
may have been less able to escape from predators. This decrease
could be the result of the energetic burden of the parasite, as
Anderson (1975) found that the metabolism of parasitized shrimp is
depressed. Instead, parasitized shrimp might attempt to escape
predation using less energy-intensive behaviors such as swimming
or remaining motionless. Bass and Weis (1999) also found that
parasitized shrimp were less active than unparasitized shrimp, but
Chaplin-Ebanks and Curran (2005) found that Probopyrus pandalicola
did not affect shrimp activity level in the absence of a predator.
Parasitized and marked shrimp were more noticeable than
unparasitized shrimp, which resulted in their preferential
consumption by the visual predator Fundulus heteroclitus. Similarly,
Bakker et al. (1997) found that more freshwater amphipods
Gammarus pulex were consumed if the painted spots imitating the
parasite Pomphorhynchus laevis were bright orange, as opposed to
matching the carapace of the amphipod.
Probopyrus pandalicola alters predator-prey dynamics in estuarine
ecosystems by affecting the behavior and camouflage of its terminal
shrimp host, as well as by decreasing shrimp reproduction through
sexual sterilization.
*
The daggerblade grass shrimp Palaemonetes pugio is an abundant
detritivore in estuarine ecosystems on the East and Gulf coasts of
the US (Welsh, 1975). Predators of grass shrimp include the Atlantic
croaker Micropogonias undulatus and the striped bass Morone saxatilis
(Clark et al., 2003).
Grass shrimp are preyed upon by visual predators such as the
mummichog Fundulus heteroclitus (Clark et al., 2003). Backward
thrusting is an anti-predatory shrimp behavior that can permit
escape (Morgan, 1987) but increases visibility (Smith and Weis,
1997). Swimming, walking, and remaining motionless are the most
common shrimp behaviors (Kunz et al., 2006). Grass shrimp are
normally well camouflaged because of their transparent
exoskeletons and body tissues (Bhandiwad and Johnsen, 2011).
More than 16 palaemonid shrimps are sexually sterilized by the
hematophagous bopyrid isopod parasite Probopyrus pandalicola
(Kensley and Schotte, 1989). The branchial chamber of an infected
shrimp contains a female-male pair of isopods (Figure 1) (Anderson
and Dale, 1981). Bopyrids have opaque black oostegites, which may
affect the camouflage of their terminal shrimp hosts.
This bopyrid affects shrimp metabolism (Anderson, 1975), survival
during starvation (Sherman and Curran, 2013), and tolerance to
insecticides (Williamson et al., 2009). Bass and Weis (1999) found
that parasitized shrimp were less active than unparasitized shrimp,
but Chaplin-Ebanks and Curran (2005) found that Probopyrus
pandalicola did not affect shrimp activity level.
185
Table 1. The number of daggerblade grass shrimp Palaemonetes pugio that were
consumed by the mummichog Fundulus heteroclitus in 2.5 L aquaria as a
function of whether they were unparasitized, parasitized by the bopyrid
isopod Probopyrus pandalicola, or marked. An * indicates a significant
difference between types of shrimp within a treatment.
Figure 4. Consumption of all types of daggerblade grass shrimp Palaemonetes
pugio (n=203 shrimp) that were consumed by the mummichog Fundulus
heteroclitus as a function of shrimp behavior immediately prior to
consumption in 2.5 L aquaria. An * indicates a significant difference between
shrimp that were consumed and those that were not consumed.
0
20
40
60
80
Motionless Walking Swimming Backward
thrusting
Percent of shrimp
Consumed Not consumed
*
*
*
*
Figure 1. Female (♀) and male (♂)
Probopyrus pandalicola (2-4 mm) in
the branchial chamber of a
Palaemonetes pugio
Figure 2. A typical mummichog Fundulus
heteroclitus (5-10 cm TL) and unparasitized grass
shrimp Palaemonetes pugio (2-4 cm TL) in an
experimental aquarium
L. Bruen B. Brinton B. Brinton
Unparasitized shrimp Parasitized shrimp Marked shrimp
L. Bruen
L. Bruen
Treatment/Potential Effect(s) Shrimp Consumed
Behavior and/or Camouflage
Parasitized (51)
*
Unparasitized (34)
*
Behavior
Parasitized (6)
Marked (2)
Camouflage
Marked (8)
Unparasitized (4)
Figure 3. The effect of the relative behavior and camouflage of the
daggerblade grass shrimp Palaemonetes pugio on whether it was consumed by
the mummichog Fundulus heteroclitus in 2.5 L aquaria. The categories indicate
whether the consumed shrimp was the more, equally, or less active shrimp of
the pair. An * indicates a significant difference between more camouflaged
and less camouflaged shrimp.
0
10
20
30
40
50
60
70
80
More active Equally active Less active
Percent of shrimp consumed
Relative activity
More camouflaged Less camouflaged
*
Unparasitized Marked Parasitized
