1 23

HydrobiologiaThe International Journal of AquaticSciences ISSN 0018-8158Volume 720Number 1 Hydrobiologia (2013) 720:101-110DOI 10.1007/s10750-013-1628-0

Effect of light, prey density, and prey typeon the feeding rates of Hemimysis anomala

Kathleen E. Halpin, Brent T. Boscarino,Lars G. Rudstam, Maureen G. Walsh &Brian F. Lantry

1 23

Your article is protected by copyright and all

rights are held exclusively by Springer Science

+Business Media Dordrecht. This e-offprint

is for personal use only and shall not be self-

archived in electronic repositories. If you wish

to self-archive your article, please use the

accepted manuscript version for posting on

your own website. You may further deposit

the accepted manuscript version in any

repository, provided it is only made publicly

available 12 months after official publication

or later and provided acknowledgement is

given to the original source of publication

and a link is inserted to the published article

on Springer's website. The link must be

accompanied by the following text: "The final

publication is available at link.springer.com”.

PRIMARY RESEARCH PAPER

Effect of light, prey density, and prey type on the feedingrates of Hemimysis anomala

Kathleen E. Halpin • Brent T. Boscarino •

Lars G. Rudstam • Maureen G. Walsh •

Brian F. Lantry

Received: 6 February 2013 / Revised: 1 July 2013 / Accepted: 20 July 2013 / Published online: 3 August 2013

� Springer Science+Business Media Dordrecht 2013

Abstract Hemimysis anomala is a near-shore mysid

native to the Ponto-Caspian region that was discov-

ered to have invaded Great Lakes ecosystems in 2006.

We investigated feeding rates and prey preferences of

adult and juvenile Hemimysis in laboratory experi-

ments to gain insight on the potential for Hemimysis to

disrupt food webs. For both age groups (AGs), we

measured feeding rates as a function of prey abun-

dance (Bosmina longirostris as prey), prey type (B.

longirostris, Daphnia pulex, and Mesocyclops sp.),

and light levels (no light and dim light). Mean feeding

rates on Bosmina increased with prey density and

reached 23 ind. (2 h)-1 for adults and 17 ind. (2 h)-1

for juveniles. Dim light had little effect on prey

selection or feeding rate compared to complete

darkness. When feeding rates on alternate prey were

compared, both AGs fed at higher rates on Bosmina

than Daphnia, but only juveniles fed at significantly

higher rates on Bosmina relative to Mesocyclops. No

significant differences were observed between feeding

rates on Mesocyclops and on Daphnia. Hemimysis

feeding rates were on the order of 30–60% of their

body weight per day, similar to predatory cladocerans

that have been implicated in zooplankton declines in

Lakes Huron and Ontario.

Keywords Hemimysis � Feeding rates � Prey

selection � Great Lakes

Introduction

A considerable increase in the global shipping trade

has caused an influx of invasive species into aquatic

habitats worldwide. Many of these invasive species

have established populations in the United States and

caused damage to the environment, human health, and

industry (Mills et al., 1994). The Great Lakes have

received over 180 invasive species since 1840

(Ricciardi, 2006), many of which were unintentionally

introduced via ship ballast water (Holeck et al., 2004).

Hemimysis anomala (hereafter referred to as Hemim-

ysis) is a recent invader that originated from the

Handling editor: Karl E. Havens

K. E. Halpin � B. T. Boscarino � L. G. Rudstam (&)

Department of Natural Resources, Cornell Biological

Field Station, Cornell University, 900 Shackelton Point

Road, Bridgeport, NY 13030, USA

e-mail: lgr1@cornell.edu

K. E. Halpin

e-mail: kh387@cornell.edu

B. T. Boscarino

e-mail: btb32@cornell.edu

M. G. Walsh � B. F. Lantry

Biological Resources Division, Lake Ontario Biological

Station, U.S. Geological Survey, 17 Lake Street, Oswego,

NY 13126, USA

e-mail: mwalsh@usgs.gov

B. F. Lantry

e-mail: bflantry@usgs.gov

123

Hydrobiologia (2013) 720:101–110

DOI 10.1007/s10750-013-1628-0

Author's personal copy

Ponto-Caspian region of Eurasia and was most likely

introduced to the Great Lakes through ballast water

discharge (Koops et al., 2010). This mysid species was

first observed in Lake Ontario near Oswego, NY and in

Lake Michigan near Muskegon, MI in 2006 (Walsh

et al., 2010). Its relatively high and sustained abun-

dances in four of the five Great Lakes (none have yet

been observed in Lake Superior) and its establishment

in inland lakes in New York State since 2009

(Brooking et al., 2010; Brown et al., 2012) indicates

that the species is thriving and spreading within the

Great Lakes Basin.

The potential role of Hemimysis in Great Lakes

food webs is largely unknown. The establishment of

Hemimysis in invaded systems in Europe has been

associated with substantial decreases in cladoceran

and copepod abundances in reservoirs in the Nether-

lands (Ketelaars et al., 1999) and gravel pit lakes near

the Rhine River (Borcherding et al., 2006). Thus, it is

likely that Hemimysis can alter zooplankton species

composition in invaded North American systems and,

therefore, affect other planktivores dependent on those

prey resources. In addition, Hemimysis is primarily a

nearshore predator whereas other major invertebrate

zooplankton predators (Mysis diluviana, Bythotrephes

longimanus, and Cercopagis pengoi) are mainly found

offshore (Walsh et al., 2012). Thus, Hemimysis adds a

new spatial dimension to invertebrate zooplanktivory

in the Great Lakes and elsewhere (Borcherding et al.,

2006; Boscarino et al., 2012). At the same time,

Hemimysis are consumed by various fish species.

Borcherding et al. (2006) and Stich et al. (2009) found

that Hemimysis have become a quality food source for

fish in reservoirs near the Rhine River in Germany, and

Lantry et al. (2010, 2012) documented Hemimysis in

the diets of Lake Ontario alewife, Alosa pseudoha-

rengus; yellow perch, Perca flavescens; rock bass,

Ambloplites rupestris; cisco, Coregonus artedi; and

white perch, Morone americana.

The degree to which Hemimysis will impact native

zooplankton abundances in invaded ecosystems will

depend on feeding rates, feeding success, and prey

availability. Smaller mysids utilize phytoplankton,

benthic diatoms, rotifers, and detritus as their primary

food sources (Viherluoto & Viitasalo, 2001). As

mysids grow and their swimming ability increases,

they include larger cladocerans and copepods in their

diets (Viherluoto et al., 2000; Lehtiniemi & Nord-

strom, 2008). According to Viherluoto et al. (2000)

Mysis mixta shifted from feeding primarily on benthic

sedimentary diatoms to feeding on zooplankton as

they increased in size from June through September.

Prey items that make up a mysid’s carnivorous diet can

be ingested whole (Lehtiniemi & Nordstrom, 2008)

but can also show a high degree of prey fragmentation,

especially in the diets of adults (e.g., Grossnickle,

1982). Mysids generally select cladocerans over

copepods, likely because copepods are better able to

detect mysids and/or escape after an encounter

(Mohammadian et al., 1997; Viitasalo et al., 1998;

Viherluoto & Viitasalo, 2001). Similar to other mysids,

size-selective feeding and a shift to a more carnivorous

diet with age has been reported for Hemimysis (Marty

et al., 2010).

Light conditions may also affect Hemimysis feed-

ing success. Boscarino et al. (2012) showed that

Hemimysis is found on the bottom during the day,

preferring rocky habitats with relatively small inter-

stitial spaces where it can hide (Claramunt et al.,

2012). Then, as early as civil twilight, Hemimysis

begins to migrate into the water column. Juveniles

prefer higher light levels (LLs) than adults, and thus

begin their vertical migration earlier than adults

(Boscarino et al., 2012). Mysids generally use both

visual and tactile cues to detect prey; but the extent to

which light enhances feeding rate in mysids is likely

size- and species-dependent (Viitasalo et al., 1998;

Viherluoto & Viitasalo, 2001). For example, a study

comparing a littoral mysid, Praunus flexuosus, and a

pelagic mysid, Mysis mixta, revealed that light does

not affect the feeding rates of the littoral P. flexuosus;

however, it does negatively affect the feeding rate of

the pelagic M. mixta (Viherluoto & Viitasalo, 2001).

Ramcharan & Sprules (1986) showed that predation

rates of M. diluviana increased during LLs corre-

sponding to a full moon. Therefore, we also tested two

LLs for both age groups (AGs)—the first being

complete darkness, and the second dim light encoun-

tered by juvenile mysids during twilight (about

160 lux, Boscarino et al., 2012).

In this study, we investigated (1) Hemimysis

feeding rates as a function of prey density (PD) (using

Bosmina longirostris as prey); (2) feeding rates as a

function of prey type (comparing feeding rates on

Bosmina, Daphnia pulex, and Mesocyclops sp. when

prey were offered in separate containers); and (3) prey

selection when presented these three prey types in the

same container. All experiments were done with two

102 Hydrobiologia (2013) 720:101–110

123

Author's personal copy

AGs (adults and juveniles) and at two LLs (darkness

and dim light *160 lux). We expected that the

feeding rates of Hemimysis would increase with

increasing prey densities up to an asymptote repre-

senting maximum consumption rates for both age

classes, that Hemimysis would feed at higher rates on

the less evasive cladocerans than copepods for both

age classes, and that Hemimysis would select for

cladocerans over copepods when given a choice of

these prey in the same container. We also hypothe-

sized that adult Hemimysis would have higher feeding

rates than juveniles regardless of LL, and that feeding

rates would be higher in dim light than in the dark.

This is the first study to: (a) derive a functional

response curve for Hemimysis feeding at varying prey

densities, (b) determine prey preference under con-

trolled conditions, and (c) determine the effect of light

on feeding rate and prey preference under controlled

conditions.

Materials and methods

Collection and maintenance

Live Hemimysis were collected for use in laboratory

experiments in June and July 2010 using vertical and

horizontal net hauls off the Stiver’s Marina pier on

Seneca Lake in Geneva, New York. The bottom depth

at this site was 3 m. We used an 800-lm-mesh net and

retrieved the net at a rate of 0.3 m s-1 after Boscarino

et al. (2012). The collected organisms were immedi-

ately placed into several 2- to 3-l plastic containers

filled with lake water and brought back to the Cornell

Biological Field Station in Bridgeport, New York

in insulated coolers. Laboratory conditions were

designed to resemble those experienced by Hemimysis

in the field. The mysids were kept in a temperature-

controlled room set to 16�C to mimic the temperature

at the time of collection. Each room had a 14 h:10 h

dark:light cycle and were fed Cyclop-eez� (a labora-

tory-developed food source similar to Artemia nauplii

in nutritional value) on a daily basis (Boscarino et al.,

2012). Ammonia levels were checked daily and the

water was exchanged (dechlorinated municipal water

from Lake Ontario) every 7 days. LLs were approx-

imately 160 lux, which represents LLs similar to those

at the surface at sunset or early civil twilight when

Hemimysis vertically migrates into the water column

from daytime hiding places (Boscarino et al., 2012).

Hemimysis were not starved prior to experimentation

to avoid unnaturally high feeding rates.

Immediately following a feeding experiment,

experimental Hemimysis were euthanized and mea-

sured from the tip of the rostrum to the end of the

abdomen. The telson and caudal plates were not

included in this measurement, following the measur-

ing techniques from Boscarino et al. (2012) and the

standard operating procedures for the Department of

Fisheries and Oceans Canada (Koops et al., 2010).

Juveniles were defined as any organism B4.5 mm and

adults as [4.5 mm in length (after Boscarino et al.,

2012). We used a Motic� dissecting microscope with

a PixelLINK� camera attachment and imaging soft-

ware to measure the organisms. The sex of the adult

Hemimysis was confirmed by the presence or absence

of a fourth elongated pleopod (male) or a brood sac

(female).

Prey density experiments

The purpose of this experiment was to determine the

effect of PD on the predation rate of juvenile and adult

Hemimysis under different light conditions. The prey

used in this experiment, Bosmina longirostris (here-

after Bosmina), was collected from a pier off Shac-

kelton Point on Oneida Lake, New York during June–

July 2010. To determine the average length of

Bosmina at this site, we took a random subsample

from the collection that we used in the experiments

and measured the length of individual bosminids from

the top of the head to the base of the caudal spine

(following the standard operating procedure for Cor-

nell Biological Field Station, as summarized in

Watkins et al. (2011)). The average length of these

Bosmina was 0.31 mm (n = 54, SD = 0.07). Bos-

mina was selected because they are abundant in most

systems that Hemimysis inhabits, have been found in

the stomachs of Hemimysis from Lake Ontario (Walsh

et al., unpublished data), and experienced high rates of

predation by Hemimysis in a European reservoir

(Ketelaars et al., 1999).

Prior to experimentation, the Bosmina was kept in

19-l aquaria in a 20�C temperature-controlled exper-

imental room, as this was the temperature of the lake

when they were collected. Bosmina is strongly

Hydrobiologia (2013) 720:101–110 103

123

Author's personal copy

phototactic relative to other zooplankton and individ-

ual Bosmina were separated from the stock container

by shining a light in one corner and pipetting them out

into a smaller jar. Individual Bosmina were then

suctioned out of that jar with a smaller pipette that was

next placed under a dissecting microscope where the

number of Bosmina in the pipette was counted. If other

species were found in the pipette, the water was

discarded. Five, 10, 20, 30, and 50 Bosmina were then

transferred to 750-ml square containers filled with

0.5 l of filtered water from Oneida Lake.

One individual Hemimysis placed into an experi-

mental container with Bosmina represented one rep-

licate. Ten replicates and two controls (treated in the

same manner as the experimental containers but

without the added Hemimysis) were run for 2 h for

each density treatment and Hemimysis AG in both

dark and light (*160 lux) conditions (Table 1).

Preliminary experiments indicated that this time

period allowed mysids to consume at least half of

the available prey at each PD. At the end of the 2-h

feeding period, the animals were checked to ensure

that they were still alive and the water was filtered onto

a standard filter paper (particle retention 1.5 lm). The

individual Hemimysis was removed and measured.

The experimental container and the top reservoir of the

water filter were then rinsed twice to ensure that all

remaining prey organisms were flushed onto the filter

paper. The filter paper was removed and placed on a

Petri dish. The number of Bosmina on the filter paper

was determined using a dissecting microscope at

1209 magnification. For all 20 controls, the number of

Bosmina found at the end of the experiment was the

same as the number initially introduced confirming the

effectiveness of the filtering and counting methodol-

ogy. Feeding rates were, therefore, calculated by

subtracting the number of organisms counted by the

number originally placed in the feeding containers and

reported as the number eaten (2 h)-1. Few animal

fragments were found; those animals were counted as

‘‘eaten.’’ Statistical analyses of the effect of AG, LL,

and PD on feeding rates were done using a General

Linear Model (GLM) on square-root transformed

feeding rates (Jmp ver 9.1). Two-way interaction

terms were included when appropriate.

After all analyses were completed, we generated a

Type II functional response curve based on the mean

feeding rates obtained for each AG–LL combination

using the standard formula:

F ¼ Vmax Dð Þ Km þ Dð Þ�1� �� �

;

where F is feeding rate in no. predator-1 2 h-1, D is

prey density in no. l-1, Vmax is the extrapolated

maximum feeding rate, and Km is the extrapolated

half-saturation constant. The curve was generated with

a non-linear fit by minimizing the squared deviation.

Prey-type experiments

In this set of experiments we compared Hemimysis

predation rates on different prey species (Daphnia

pulex, and mixed Mesocyclops sp., hereafter Mesocy-

clops and Daphnia, respectively) at the same two LLs

and Hemimysis AGs as described in the PD experi-

ments. Predation rates on Mesocyclops and Daphnia

were compared to the predation rates on Bosmina

determined in the PD experiments. Daphnia and

Mesocyclops were obtained from Sachs Systems

Aquaculture�. The average length of an individual

Daphnia was 1.56 mm (measured from top of head to

base of caudal spine, n = 15, SD = 0.66) and the

average size of Mesocyclops was 1.06 mm (measured

from top of head to base of caudal spine, n = 33,

SD = 1.03). All prey organisms were kept in climate-

controlled rooms in their own 2-l containers prior to

experimentation. They were fed with a Roti-Rich�solution. The same methodology for separating and

counting these organisms was used as in the PD

feeding rate experiments. Twenty prey organisms

were placed in each experimental container (density of

20 ind. 0.5 l-1) with one Hemimysis for 2 h. At least

eight replicate runs and two controls were performed

for each Hemimysis AG, light condition, and prey type

(Table 1). Preliminary experiments indicated that this

time period allowed mysids to consume about half of

the available prey at this PD. Statistical analyses of the

effect of AG, LL, and prey type on feeding rates were

done using a GLM on square-root transformed feeding

rates as with the PD experiment.

Prey selection experiment

Prey selectivity by Hemimysis was investigated by

offering 20 individuals of each of three species

(Bosmina, Daphnia, and Mesocyclops) per 0.5-l

experimental container, for a total of 60 prey items

per container (Table 1); Hemimysis prey selection was

104 Hydrobiologia (2013) 720:101–110

123

Author's personal copy

Table 1 Experimental results from the PD, prey-type and prey selection experiments

Prey type Initial PD AG LL n No. of prey

eaten (range)

Mean proportion

consumed (range)

Significance

PD experiment

Bosmina 5 Ad Light 10 1.4 (0–3) 0.28 (0.00–0.60) H

5 Ad Dark 10 1.8 (0–4) 0.36 (0.00–0.80) G, H

10 Ad Light 10 3.0 (1–6) 0.30 (0.00–0.60) F, G, H

10 Ad Dark 10 5.4 (3–9) 0.54 (0.30–0.90) D, E, F, G

20 Ad Light 9 8.9 (4–13) 0.44 (0.20–0.65) B, C, D, E

20 Ad Dark 10 8.3 (3–12) 0.42 (0.15–0.60) C, D, E

30 Ad Light 10 12.1 (5–26) 0.40 (0.17–0.87) B, C, D

30 Ad Dark 10 10.6 (5–17) 0.35 (0.17–0.57) B, C, D

50 Ad Light 10 23.0 (12–39) 0.46 (0.24–0.78) A

50 Ad Dark 10 16.1(8–23) 0.34 (0.16–0.46) A, B

5 Juv Light 10 1.5 (0–3) 0.30 (0.00–0.60) H

5 Juv Dark 10 2.5 (0–3) 0.50 (0.20–1.00) F, G, H

10 Juv Light 10 3.8 (1–8) 0.38 (0.10–0.80) E, F, G, H

10 Juv Dark 10 5.5 (2–8) 0.55 (0.20–0.80) D, E, F

20 Juv Light 9 6.4 (2–18) 0.32 (0.10–0.90) D, E, F

20 Juv Dark 10 8.3 (4–11) 0.42 (0.15–0.55) C, D, E

30 Juv Light 10 11.5 (4–17) 0.38 (0.13–0.57) B, C, D

30 Juv Dark 10 12.8 (6–17) 0.43 (0.20–0.57) B, C

50 Juv Light 8 16.8 (15–22) 0.34 (0.06–0.44) A, B

50 Juv Dark 10 16.2 (6–24) 0.32 (0.12–0.48) A, B

Prey-type experiment

Bosmina 20 Ad Light 9 8.9 (4–13) 0.44 (0.20–0.65) A

20 Ad Dark 10 8.3 (3–12) 0.42 (0.15–0.60) A, B

Mesocyclops 20 Ad Light 10 6.6 (0–12) 0.33 (0.05–0.60) A, B

20 Ad Dark 10 7.3 (1–12) 0.37 (0.05–0.60) A, B

Daphnia 20 Ad Light 10 5.1 (1–11) 0.26 (0.05–0.55) A, B

20 Ad Dark 9 6.3 (3–13) 0.32 (0.15–0.65) A, B

Bosmina 20 Juv Light 9 6.4 (2–9) 0.32 (0.10–0.90) A, B

20 Juv Dark 10 8.3 (3–11) 0.42 (0.15–0.55) A

Mesocyclops 20 Juv Light 10 3.9 (1–8) 0.20 (0.05–0.40) A, B

20 Juv Dark 9 4.3 (0–8) 0.22 (0.00–0.40) A, B

Daphnia 20 Juv Light 8 3.3 (1–7) 0.14 (0.05–0.35) A, B

20 Juv Dark 10 4.4 (0–8) 0.22 (0.00–0.40) B

Prey selection experiment

Bosmina 20 Ad Light 6 7.2 (5–9) 0.36 (0.25–0.45) A, B

20 Ad Dark 6 8.0 (4–11) 0.40 (0.20–0.55) A, B

Mesocyclops 20 Ad Light 6 3.0 (0–6) 0.15 (0.00–0.30) B, C

20 Ad Dark 6 1.5 (0–6) 0.08 (0.00–0.30) C

Daphnia 20 Ad Light 6 7.7 (3–9) 0.38 (0.15–0.45) A, B, C

20 Ad Dark 6 7.8 (0–14) 0.39 (0.00–0.70) A, B, C

Bosmina 20 Juv Light 6 10.0 (2–14) 0.50 (0.10–0.70) A

20 Juv Dark 6 8.3 (2–16) 0.42 (0.10–0.80) A, B, C

Hydrobiologia (2013) 720:101–110 105

123

Author's personal copy

determined by counting the remaining numbers of

each prey type at the end of the experiment and

comparing them across treatment groups. Experiments

were run at both dark and dim light conditions with

one adult or juvenile Hemimysis added to each

container and allowed to feed for 2 h. After 2 h, the

individual Hemimysis was removed and remaining

prey were sorted and counted in the same manner as in

previous experiments. At least five replicates were

performed in the light and five in the dark for each

Hemimysis AG. No controls were performed for this

experiment because previous experiments had

revealed a high level of reliability in the counting

method. Selectivity was calculated using the Ches-

son’s alpha index (ai) (Chesson, 1978):

at ¼ ri=pið Þ=X

k

ri=pi

!;

where ri, is the proportion of prey i in the stomach and

pi, is the proportion of prey i in the lake. We tested for

differences in this selectivity index between prey

types, mysid AGs, and LLs. Since our experiments

involved three prey types, neutral selection is at

ai = 0.33. Statistical analyses on feeding rates were

performed as in the prey-type experiment.

Results

Prey density experiment

A total of 196 trials were conducted using different prey

densities (5, 10, 20, 30, and 50 prey 0.5 l-1), two

LLs (dark and dim light), and two AGs (adults and

juveniles). The number of replicates for each treatment

ranged from 8 to 10 (Table 1) as we excluded any

experiments that did not have an actively swimming

Hemimysis present at the end of the feeding trial. Adult

Hemimysis averaged 6.1 mm (range 5.7–6.7 mm)

and juveniles 3.4 mm (range 3.0–4.0 mm) in these

experiments.

Feeding rates (FR, prey 2 h-1 Hemimysis-1) aver-

aged 16.1 (dark) to 23.0 (light) Bosmina for adults and

16.2 (dark) to 16.8 (light) Bosmina for juveniles at the

highest PD (50 prey 0.5 l-1). LL and AG were not

significant predictors of feeding rate alone (P = 0.13

and 0.73, respectively). There was a significant

interaction between PD and LL (P = 0.0035) owing

to the higher feeding rates of adults in dim light at the

0

5

10

15

20

25

0 10 20 30 40 50 60 70 80 90 100

Bos

min

a2h

-1

Initial prey density (Bosmina L-1)

Observed

FR II

Fig. 1 Feeding rates (no. Bosmina eaten 2 h-1) as a function of

PD in the PD experiments. Please note that the x-axis has been

extrapolated to initial PD l-1 but that feeding trials were done in

0.5-l containers over a 2-h trial. The curve represents the best fit

Type II functional response curve (FR II) using the results of

each treatment combination as the input data. Mean feeding

rates through which the curve was fit represent a pooled mean

from both light and age treatments for that particular density

group

Table 1 continued

Prey type Initial PD AG LL n No. of prey

eaten (range)

Mean proportion

consumed (range)

Significance

Mesocyclops 20 Juv Light 6 3.7 (0–10) 0.18 (0.00–0.50) B, C

20 Juv Dark 6 5.3 (3–8) 0.27 (0.15–0.45) A, B, C

Daphnia 20 Juv Light 6 3 (1–5) 0.13 (0.05–0.25) B, C

20 Juv Dark 6 4.7 (0–9) 0.23 (0.00–0.45) A, B, C

Initial prey densities are reported in number of prey in a 0.5-l container. Feeding trials were run over a 2-h time period and the

number of prey eaten is given for the 2-h period. In prey-type experiments, prey were fed to Hemimysis separately, and in prey

selection experiments, all three prey were offered at once. Different letters in the ‘‘significance’’ column signify that mean

proportions of prey consumed were significantly different from each other (Tukey’s HSD, a = 0.05) within experiment type (density,

type, selection). For each experiment type, results at each LL are reported for adult Hemimysis first (Ad), followed by results for

juvenile Hemimysis (Juv)

106 Hydrobiologia (2013) 720:101–110

123

Author's personal copy

highest PD combined with higher feeding rates of both

age classes in the dark at lower prey densities

(Table 1). Therefore, when we analyzed feeding rate

as a function of PD and LL, we ran separate

regressions for the light and the dark treatment. These

models for feeding rate were highly significant for

both LLs (dark: F3,95 = 59.5; P \ 0.0001; adjusted

R2 = 0.65, light: F3,91 = 70.3; P \ 0.0001; adjusted

R2 = 0.78, Fig. 1) and there was no significant

AG 9 PD interactions. At both LLs, feeding rate

increased significantly with PD (P \ 0.0001) whereas

the AG effect was not significant (dark: P = 0.33,

light: P = 0.09).

The Type II functional response curve fitted to this

data had a maximum feeding rate (Vmax) of 38.5

Bosmina 2 h-1 (SE = 4.08) and a half-saturation

constant (Km) of 138.7 Bosmina l-1 (SE = 22.02)

(R2 = 0.91, Fig. 1).

Prey-type experiment

Feeding rates on Daphnia and Mesocyclops were

compared with feeding rates on Bosmina from the PD

experiments at the 20 Bosmina 0.5 l-1 density level.

There was a significant effect of prey type (P \ 0.0001)

and mysid AG (P \ 0.0029) on feeding rates but no

effect of LLs (P = 0.21) and no 2-way interactions

were significant (P = 0.18) (general linear regression;

F4,109; F-stat = 7.35; n = 114; P \ 0.0001); however,

the amount of variability explained by the complete

model was relatively low (R2 = 0.21). Mean feeding

rates (±1 SE) of adults (in prey 2 h-1) were signifi-

cantly higher than feeding rates of juveniles (7.1 and

5.1, respectively; P = 0.003) and mean feeding rates on

Bosmina were significantly higher than on Mesocyclops

(8.0 and 5.5, respectively; P = 0.006) or on Daphnia

(mean prey (2 h-1) = 4.8; P \ 0.0001); however, no

significant differences in feeding rates were found for

Hemimysis consuming Daphnia or Mesocyclops

(P = 0.58) (Fig. 2).

Prey selection experiment

Hemimysis feeding rates were affected by the combi-

nation of Hemimysis AG and prey type (P \ 0.0005)

but not by LL (P = 0.78, Table 1). Therefore, we

combined LLs. However, few comparisons were

significant (Tukey’s HSD test, Table 1). Adults con-

sumed Bosmina and Daphnia and juveniles consumed

Bosmina at higher rates than copepods.

Selection by adult Hemimysis was similar for both

Bosmina and Daphnia in both light and dark conditions

(Chesson’s a = 0.43 and 0.43, respectively, in light,

and a = 0.48 and 0.42, respectively, in dark) (Fig. 3).

Mesocyclops was selected against in both light and

dark experiments (a = 0.15 in light and 0.10 in dark).

Juvenile Hemimysis in dim light was selected for

Bosmina (a = 0.63) and against Daphnia (a = 0.15)

and Mesocyclops (a = 0.22). In the dark, juvenile

Hemimysis showed only small differences in

0123456789

10

Bosmina Mesocyclops Daphnia

No.

pre

y (2

h)-1

, +

/-1

SE

Juvenile

Adult

A B* B *

Fig. 2 Comparison of mean numbers of prey eaten in 2-h

feeding trials by both juvenile and adult Hemimysis in the prey-

type experiment. Error bars are ±1 SE. Both AGs ate

significantly more Bosmina than the other two prey types, as

indicated by different letters above paired means. An asterisk

indicates that the mean number of prey was significantly

different between adults and juveniles for that prey type

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Bosmina Mesocyclops Daphnia

Che

sson

's al

pha

inde

x

adult light

adult dark

juvenile light

juvenile dark

Fig. 3 Mean Chesson’s alpha index values from the prey

selectivity experiment. Error bars are ±1 SE. A value of 0.33

represents neutral selection for any of the three prey types,

values above 0.33 represent positive selection, and values below

0.33 represent selection against a certain prey type

Hydrobiologia (2013) 720:101–110 107

123

Author's personal copy

selectivity (a = 0.36 for Bosmina, 0.32 for Daphnia,

and 0.32 for Mesocyclops).

Discussion

Our experimental results provide insights into feeding

rates and prey selection of the recent invader,

Hemimysis, that will help us understand the ecological

role of this species in their new environment and

inform future field-based research. In our experiments,

Hemimysis feeding rates continued to increase with

increasing initial prey (Bosmina) density up to the

highest PD tested (50 ind. container-1, equivalent to

100 Bosmina l-1). Feeding rates of adults were higher

than those of juveniles when feeding on larger prey

(Daphnia and Mesocyclops) but not when feeding on

Bosmina. Our observed feeding rates are similar to

results for other small mysid species. Fulton (1982), in

a 24-h experiment, determined saturation levels (the

point at which predation becomes independent of PD)

for Mysidopsis bigelowi as over 100 individual Acartia

tonsa copepods and up to 50 individual Centropages

sp. copepods in one-liter containers. Chigbu & Sibley

(1994) showed that Neomysis mercedis can ingest up

to 30 small Daphnia in 12-h experiments. Assuming

feeding rates were constant through the longer obser-

vation periods, these literature values correspond to

2–5 copepods and Daphnia (2 h-1), which is similar to

our results.

Hemimysis fed at higher rates on Bosmina than on

copepods when given these prey alone, and selected

for Bosmina over copepods when given both prey

together. The results for Daphnia were less clear.

Feeding rates of adult Hemimysis on Daphnia were

similar to the feeding rates on Bosmina. Both cladoc-

erans were selected for over copepods in the selection

trials. However, juvenile Hemimysis fed at lower rates

on Daphnia than on Bosmina and did not select for

Daphnia in selection trials. These results suggest that

juvenile Hemimysis have difficulty feeding on Daph-

nia. Wuerstle (2011) also found that juvenile Hemim-

ysis fed at lower rates than adults when offered

Daphnia as prey. In the same experiment, Wuerstle

found that juveniles only fed on the smallest Daphnia

given. Similar results have been found for Hemimysis

(Ketelaars et al., 1999) and for Neomysis mercedis

(Murtaugh, 1981; Chigbu & Sibley, 1994). Indeed,

most studies of prey selection in different mysid

species show that these predators select cladocerans

over copepods (review by Rudstam, 2009), which is

likely due to the higher escape ability of copepods

(Viitasalo & Rautio, 1998).

Since Hemimysis perform diel vertical migrations,

we only conducted experiments at LLs they are likely

to experience during their twilight and nighttime

pelagic period. Boscarino et al. (2012) determined that

at brighter LLs, Hemimysis generally avoid the water

column but see de Lafontaine et al. (2012). Dim light

had little effect on prey selection or feeding rate

compared to complete darkness in our experiments.

Elsewhere, Viherluoto & Viitasalo (2001) observed

suppressed feeding rates on a pelagic mysid in lighted

experiments because light triggered an internal cue to

decrease movement that is likely to decrease detection

by fish. However, the dim LLs used in these exper-

iments (*160 lux) did not elicit avoidance behaviors

in Hemimysis (Boscarino et al., 2012) which contrib-

uted to the lack of a light effect on feeding rates. We do

not exclude the possibility that feeding rates would

decline at higher LLs.

Increasing container size can increase mysid feed-

ing rates in experiments (Gorokhova & Hansson,

1997), and we acknowledge that our container sizes

were relatively small. However, the mysids used here

were also small compared to Mysis mixta discussed by

Gorokhova & Hansson (1997) and our chamber size

allowed us to use experimental prey densities that

were comparable to densities found in Lake Ontario

(Holeck et al., 2008). We have not investigated if

feeding rates would be even higher if we had used

larger container sizes.

These results have important implications for the

potential role of Hemimysis in Great Lakes food webs.

Hemimysis prefers cladocerans, as do other vertebrate

and invertebrate predators in the Great Lakes (Brooks

& Dodson, 1965; Grossnickle, 1982; Mills et al., 1992;

Lehman & Caceres, 1993), and are capable of high

feeding rates. If we extrapolate our 2-h feeding rates to

a 12-h feeding period, adults could consume up to 30%

of their body weights and juveniles could consume

over 60% of their body weights (based on length-

weight regressions for Hemimysis in Marty et al., 2010

and for Bosmina in Watkins et al., 2011). Such high

specific rates are comparable to the predatory cladoc-

eran Bythotrephes longirostris (Vanderploeg et al.,

1993; Schulz & Yurista, 1999) and Cercopagis pengoi

(Pichlova-Ptacnikova & Vanderploeg, 2009); species

108 Hydrobiologia (2013) 720:101–110

123

Author's personal copy

suspected of suppressing epilimnetic zooplankton in

Lake Huron and Lake Ontario (Lehman & Caceres,

1993; Warner et al., 2006; Bunnell et al., 2011). Thus,

this new invader has the potential to be an important

planktivore in areas where it becomes abundant.

Though it remains to be seen if Hemimysis will

become abundant enough to impact nearshore zoo-

plankton communities in the Great Lakes, high

localized densities of Hemimysis have been observed

in the Finger Lakes of New York, Lake Ontario and in

the St. Lawrence River (Brown et al., 2012; de

Lafontaine et al., 2012; Marty et al., 2012; Taraborelli

et al., 2012), and in these areas of high abundance it is

likely to play a significant role in food web dynamics.

Acknowledgments This research was funded by New York

Sea Grant project R/CE-28 with additional support from the

Great Lakes Fisheries Commission. We are grateful to Brian

Weidel for valuable comments on the manuscript and to Jennifer

Sun for help in the laboratory. The views expressed are those of

the author and do not necessarily reflect the views of NOAA or

USGS. The U.S. Government is authorized to produce and

distribute reprints for governmental purposes notwithstanding

any copyright notation that may appear herein. Any use of trade,

product, or firm names is for descriptive purposes only and does

not imply endorsement by the U.S. Government. This article is

Contribution 294 of the Cornell Biological Field Station and

Contribution No 1766 from the Great Lakes Science Center.

References

Borcherding, J., S. Murawski & H. Arnt, 2006. Population

ecology, vertical migration and feeding of the Ponto-Cas-

pian invader Hemimysis anomala in a gravel-pit lake

connected to the River Rhine. Freshwater Biology 51:

2376–2387.

Boscarino, B. T., K. E. Halpin, L. G. Rudstam, M. G. Walsh &

B. F. Lantry, 2012. Age-specific light preferences and

vertical migration patterns of a Great Lakes invertebrate,

Hemimysis anomala. Journal of Great Lakes Research

38(Supplement 2): 37–44.

Brooking, T. E., L. G. Rudstam, S. D. Krueger, J. R. Jackson,

A. B. Welsh & W. W. Fetzer, 2010. First occurrence of the

mysid Hemimysis anomala in an inland lake in North

America, Oneida Lake, NY. Journal of Great Lakes

Research 36: 577–581.

Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and

composition of zooplankton. Science 150: 28–35.

Brown, M. E., R. Morse & K. O’Neill, 2012. Spatial, seasonal,

and diel distribution patterns of Hemimysis anomala in

New York State’s Finger Lakes. Journal of Great Lakes

Research 38(Supplement 2): 19–24.

Bunnell, D. B., B. M. Davis, D. M. Warner, M. A. Chriscinske &

E. F. Roseman, 2011. Planktivory in the changing Lake

Huron zooplankton community: Bythotrephes consumption

exceeds that of Mysis and fish. Freshwater Biology 56:

1281–1296.

Chesson, J., 1978. Measuring preference in selective predation.

Ecology 59: 211–215.

Chigbu, P. & T. H. Sibley, 1994. Predation by Neomysis

mercedis: effects of temperature, Daphnia pulex size and

prey density on ingestion rate and size selectivity. Fresh-

water Biology 32: 39–48.

Claramunt, R. M., N. T. Barton, J. D. Fitzsimons & T. L. Gala-

rowicz, 2012. Microhabitat association of Hemimysis

anomala on fish spawning reefs in Grand Traverse Bay,

Lake Michigan. Journal of Great Lakes Research 38(Sup-

plement 2): 32–36.

de Lafontaine, Y., J. R. M. Marty & S.-P. Despatie, 2012.

Swarms of the Ponto-Caspian mysid Hemimysis anomala

in Montreal Harbour, St. Lawrence River, Canada. Journal

of Great Lakes Research 38(Supplement 2): 25–31.

Fulton, R. S., 1982. Predatory feeding of 2 marine mysids.

Marine Biology 72: 183–191.

Gorokhova, E. & S. Hansson, 1997. Effects of experimental

conditions on the feeding rate of Mysis mixta (Crustacea,

Mysidacea). Hydrobiologia 355: 167–172.

Grossnickle, N. E., 1982. Feeding habits of Mysis relicta – an

overview. Hydrobiologia 93: 101–107.

Holeck, K. T., E. L. Mills, H. J. MacIsaac, M. R. Dochoda, R.

I. Colautti & A. Ricciardi, 2004. Bridging troubled waters:

biological invasions, transoceanic shipping, and the Lau-

rentian Great Lakes. BioScience 54: 919–929.

Holeck, K. T., J. M. Watkins, E. L. Mills, O. Johannsson, S.

Millard, V. Richardson & K. Bowen, 2008. Spatial and

long-term temporal assessment of Lake Ontario water

clarity, nutrients, chlorophyll a, and zooplankton. Aquatic

Ecosystem Health and Management 11: 377–391.

Ketelaars, H. A. M., F. E. Lambregts-van de Clundert, C.

J. Carpentier, A. J. Wagenvoort & W. Hoogenboezem,

1999. Ecological effects of the mass occurrence of the

Ponto-Caspian invader, Hemimysis anomala G.O. Sars,

1907 (Crustacea: Mysidacea), in a freshwater storage res-

ervoir in the Netherlands, with notes on its autecology and

new records. Hydrobiologia 394: 233–248.

Koops, M. A., J. Gerlofsma & J. Marty, 2010. Risk assessment

of the bloody red shrimp (Hemimysis anomala) in Canada.

DFO Can. Sci. Advis. Sec. Res. Doc. 2009/107.

Lantry, B. F., M. G. Walsh, J. H. Johnson & J. E. McKenna Jr,

2010. Occurrence of the Great Lake’s most recent invader,

Hemimysis anomala, in the diet of fishes in southeastern

Lake Ontario. Journal of Great Lakes Research 36: 179–183.

Lantry, B. F., C. Gumtow, M. G. Walsh, B. Weidel, B. T. Bo-

scarino & L. G. Rudstam, 2012. Seasonal consumption of

Hemimysis anomala by fish in southeastern Lake Ontario,

2009–2010. Journal of Great Lakes Research 38(Supple-

ment 2): 73–78.

Lehman, J. T. & C. E. Caceres, 1993. Food-web responses to

species invasion by a predatory invertebrate – Bythotre-

phes in Lake Michigan. Limnology and Oceanography 38:

879–891.

Lehtiniemi, M. & H. Nordstrom, 2008. Feeding differences

among common littoral mysids, Neomysis integer, Praunus

flexuosus, and P. inermis. Hydrobiologia 614: 309–320.

Marty, J., K. Bowen, M. A. Koops & M. Power, 2010. Distri-

bution and ecology of Hemimysis anomala, the latest

Hydrobiologia (2013) 720:101–110 109

123

Author's personal copy

invader of the Great Lakes basin. Hydrobiologia 647:

71–80.

Marty, J., J. Ives, Y. de Lafontaine, S. Despatie, M. A. Koops &

M. Power, 2012. Evaluation of carbon pathways supporting

the diet of invasive Hemimysis anomala in a large river.

Journal of Great Lakes Research 38(Supplement 2): 45–51.

Mills, E. L., R. O’Gorman, J. DeGisi, R. F. Heberger & R.

A. House, 1992. Food of the alewife (Alosa pseudoha-

rengus) in Lake Ontario before and after the establishment

of Bythotrephes cederstoemi. Canadian Journal of Fisher-

ies and Aquatic Sciences 49: 2009–2019.

Mills, E. L., J. H. Leach, J. T. Carlton & C. L. Secor, 1994.

Exotic species and the integrity of the Great Lakes: lessons

from the past. BioScience 44: 666–676.

Mohammadian, M. A., S. Hansson & B. T. De Stasio, 1997. Are

marine planktonic invertebrates food limited? The func-

tional response of Mysis mixta (Crustacea, Mysidacea) in the

Baltic Sea. Marine Ecology Progress Series 150: 113–119.

Murtaugh, P. A., 1981. Selective predation by Neomysis

mercedis in Lake Washington. Limnology and Oceanog-

raphy 26: 445–453.

Pichlova-Ptacnikova, R. & H. A. Vanderploeg, 2009. The

invasive cladoceran Cercopagis pengoi is a generalist

predator capable of feeding on a variety of prey species of

different sizes and escape abilities. Fundamental and

Applied Limnology 174: 267–279.

Ramcharan, C. W. & W. G. Sprules, 1986. Visual predation in

Mysis relicta Loven. Limnology and Oceanography 31:

414–420.

Ricciardi, A., 2006. Patterns of invasion in the Laurentian Great

Lakes in relation to changes in vector activity. Diversity

and Distributions 12: 425–433.

Rudstam, L. G., 2009. Other zooplankton. In Likens, G. E. (ed.),

Encyclopedia of Inland Waters. Elsevier, Oxford:

667–677.

Schulz, K. L. & P. M. Yurista, 1999. Implications of an inver-

tebrate predator’s (Bythotrephes cederstroemi) atypical

effects on a pelagic zooplankton community. Hydrobio-

logia 380: 179–193.

Stich, H. B., A. Hoppe & G. Masier, 2009. Zooplankton com-

position in a gravel pit lake invaded by the Ponto-Caspian

mysid Hemimysis anomala G.O. Sars 1907. Aquatic

Invasions 4: 697–700.

Taraborelli, A. C., N. Jakobi, T. B. Johnson, K. Bowen & B.

T. Boscarino, 2012. Distribution, abundance and produc-

tion of Hemimysis anomala in Lake Ontario. Journal of

Great Lakes Research 38(Supplement 2): 52–57.

Vanderploeg, H. A., J. R. Liebig & M. Omair, 1993. Bythotre-

phes predation on Great Lakes’ zooplankton measured by

an in situ method – implications for zooplankton commu-

nity structure. Arch Hydrobiologia 127: 1–8.

Viherluoto, M. & M. Viitasalo, 2001. Effect of light on the

feeding rates of pelagic and littoral mysid shrimps: a trade-

off between feeding success and predation avoidance.

Journal of Experimental Marine Biology and Ecology 261:

237–244.

Viherluoto, M., H. Kuosa, J. Flinkman & M. Viitasalo, 2000.

Food utilization of pelagic mysids, Mysis mixta and M.

relicta during their growing season in the northern Baltic

Sea. Marine Biology 136: 553–559.

Viitasalo, M. & M. Rautio, 1998. Zooplanktivory by Praunus

flexuosus (Crustacea: Mysidacea): functional responses

and prey selection in relation to prey escape responses.

Marine Ecology Progress Series 174: 77–87.

Viitasalo, M., T. Kiorboe, J. Flinkman, L. W. Pedersen & A.

W. Visser, 1998. Predation vulnerability of planktonic

copepods: consequences of predator foraging strategies

and prey sensory abilities. Marine Ecology Progress Series

175: 129–142.

Walsh, M. G., B. F. Lantry, B. T. Boscarino, K. Bowen, J.

Gerlofsma, T. Schaner, R. Back, J. Questel, R. Cap, G.

Smythe, M. Goehle, B. Young, M. Chalupnicki, J.

H. Johnson & J. McKenna, 2010. Early observations on an

emerging Great Lakes invader, Hemimysis anomala, in

Lake Ontario. Journal of Great Lakes Research 36:

499–504.

Walsh, M. G., B. T. Boscarino, J. Marty & O. E. Johannsson,

2012. Mysis diluviana and Hemimysis anomala: reviewing

the roles of a native and invasive mysid in the Laurentian

Great Lakes region. Journal of Great Lakes Research

38(Supplement 2): 1–6.

Warner, D. M., L. G. Rudstam, H. Benoıt, O. E. Johannsson & E.

L. Mills, 2006. Changes in seasonal nearshore zooplankton

abundance patterns in Lake Ontario following establish-

ment of the exotic predator Cercopagis pengoi. Journal of

Great Lakes Research 32: 531–542.

Watkins, J. M., L. G. Rudstam & K. T. Holeck, 2011. Length-

weight regressions for zooplankton biomass calculations –

a review and a suggestion for standard equations. Available

at eCommons Cornell http://hdl.handle.net/1813/24566.

Accessed December 2012.

Wuerstle, J. 2011. Hemimysis anomala prey size selection.

M.Sc., Buffalo State College, Buffalo.

110 Hydrobiologia (2013) 720:101–110

123

Author's personal copy