Invasive species as a new food source: does a nudibranch predator prefer eating an invasive bryozoan?
Membranipora membranacea is an invasive bryozoan that was first found in the Gulf of Maine in 1987 and within two years became the dominant organism living on kelps. Membranipora may have become dominant so quickly because it had little competition in a relatively unoccupied niche; however, lack of predation has also probably played a major role. Where Membranipora is native, there is usually a specialist nudibranch predator that keeps the population in check. For example, in European populations, the nudibranch Polycera quadrilineata prefers Membranipora while Onchidoris muricata is known to prefer another bryozoan, Electra pilosa. Electra, Membranipora, and Onchidoris are all now found in the Gulf of Maine while Polycera is not. We tested whether Onchidoris would (1) eat Membranipora at all, (2) eat Membranipora and Electra at different rates, and (3) show a preference for eating Membranipora or Electra when given a choice. We found that Onchidoris does eat Membranipora, and it generally eats Membranipora faster than Electra. However, when given a choice, Onchidoris prefers Electra. Onchidoris typically reproduces in the spring and grows over the fall and winter, but has recently been found reproducing in the winter in New Hampshire. Although it does not survive the winter as well as Electra, Membranipora is the dominant organism living on many macroalgae in the late summer and fall. Thus, the large Membranipora food source now available in the summer and fall may allow Onchidoris to reproduce earlier.
KeywordsBryozoan Electra pilosa Invasive species Membranipora membranacea Nudibranch Onchidoris muricata Predation
While not all non-native species cause harm (Bruno et al. 2005), some of those that establish and spread have the potential to severely alter native community structure and function (e.g. Byers 2000; Grosholz et al. 2000). Invasive species can cause native species to change their resource utilization patterns (Morgan et al. 1978; Race 1982; Brenchley and Carlton 1983) and cause direct or indirect changes in food webs (Zaret and Paine 1973; Herbold and Moyle 1986). Some invasive species can even cause extinctions of native species (Clarke et al. 1984; but see Gurevitch and Padilla 2004). While many invasive species may not have such severe effects on a community, they can facilitate establishment of additional non-native species resulting in an “invasion meltdown” (Simberloff and Von Holle 1999).
The bryozoan Membranipora membranacea (hereafter Membranipora) was first noticed encrusting laminarian kelps in the Gulf of Maine in 1987 at the Isle of Shoals (Lambert 1990; Berman et al. 1992). Within a few years, Membranipora became the dominant organism living on laminarian kelps, growing over other epibionts like Electra pilosa (hereafter Electra), which is another encrusting bryozoan, and Obelia geniculata, a hydroid (Berman et al. 1992).
The evidence so far suggests that Membranipora has negative effects on its kelp hosts. Membranipora can increase the likelihood of kelp breakage by making the kelp blades more brittle and susceptible to wave damage (Dixon et al. 1981; Lambert et al. 1992; Scheibling et al. 1999), or by concentrating snail herbivory in bare blade areas (Chavanich and Harris 2000). Encrustations of bryozoans can decrease kelp growth by interfering with light absorption for photosynthesis (Wing and Clendenning 1971; Oswald et al. 1984; Cancino et al. 1987; Muñoz et al. 1991) and creating a barrier against nutrient uptake and gas exchange (Hurd et al. 1994; Hurd et al. 2000). Membranipora encrustations can also decrease kelp reproduction by reducing spore release (Saier and Chapman 2004). Healthy kelp forests prevent other canopy seaweeds from recruiting, but outbreaks of Membranipora that cause substantial losses in the kelp canopy allow the invasive green seaweed Codium fragile ssp. tomentosoides to recruit and prevent the kelps from recovering (Scheibling 2000; Levin et al. 2002; Sumi and Scheibling 2005). As a result, substantial areas of the rocky subtidal along the Atlantic coast of Nova Scotia and the Gulf of Maine have shifted from kelp dominance to C. fragile ssp. tomentosoides dominance (Harris and Tyrrell 2001; Levin et al. 2002; Mathieson et al. 2003; Theriault 2003).
While most of the research on Membranipora in the Gulf of Maine has focused on the invasive bryozoan’s negative effects on other species, little work has been done on how this species was able to spread so quickly once it became established. In general, invasive species can spread quickly once they are established because they are often better competitors for resources (Race 1982; Brenchley and Carlton 1983; Vermeij 1991; Byers 2000), have faster growth rates (Hockey and Schurink 1992; Byers 2000; Stachowicz et al. 2002), take advantage of unused or underused resources (Simberloff 1981; Roughgarden 1986), or are released from predators and pathogens (Keane and Crawley 2002; Mitchell and Power 2003; Colautti et al. 2004). Before the Membranipora invasion, kelps in the Gulf of Maine had few epibionts; thus, one reason why Membranipora was able to spread quickly was that it invaded a habitat that was largely available (Berman et al. 1992). In addition, Membranipora tends to be a strong competitor that overgrows the other typical kelp epibionts (Berman et al. 1992). Release from predation is also likely to have been important in allowing Membranipora to spread since no predators were seen consuming Membranipora in the first few years after its introduction (Lambert et al. 1992; Harris and Matheison 2000). While incidences of an association between potential predators and Membranipora have been noted (Harris and Matheison 2000; Chapman et al. 2002), no experimental studies have been conducted on predator preferences for Membranipora in the Gulf of Maine.
Many potential Membranipora predators occur in the Gulf of Maine, including dorid nudibranchs, sea urchins, snails, fish, and juvenile sea stars. Sea urchins have been shown to consume Membranipora while eating kelp, and urchins grow faster when they consume kelp covered in Membranipora than bare kelp (Nestler and Harris 1994). Where Membranipora is native, predation can play a major role regulating colony survival (Yoshioka 1982) and dorid nudibranchs tend to be the most important predators on Membranipora. On the west coast of the United States, Doridella steinbergae specializes in feeding on Membranipora (Seed 1976; Harvell 1986). In Europe, Onchidorismuricata (hereafter Onchidoris) will eat Membranipora but prefers the bryozoan Electrapilosa (Todd 1978, 1979; Chadwick and Thorpe 1981; Todd 1981; Todd and Havenhand 1989; Harris and Matheison 2000), whereas Polycera quadrilineata prefers Membranipora (Ryland 1976; Todd and Havenhand 1989). Onchidoris, Electra, and Membranipora are all currently found in the Gulf of Maine but P. quadrilineata is not. Onchidoris has been found in association with Membranipora in recent years (Harris and Matheison 2000; Chapman et al. 2002), but it is unclear whether this nudibranch is having any effect on the Membranipora population.
In the present study, we address three main questions: (1) will Onchidoris eat Membranipora, (2) does Onchidoris eat Membranipora and Electra at different rates, and (3) does Onchidoris prefer Membranipora or Electra?
Materials and methods
Bryozoan colonies are made of individual modules called zooids. Each zooid contains a polyp-like body called a polypide, which consists of the ciliated crown of feeding tentacles as well as the main body containing the gut. The polypide sits inside a protective housing (the zooecium). Zooids are budded asexually, and they remain connected physically and physiologically to create the colony. Onchidoris is a suctorial feeder, meaning it eats the polypide without destroying the zooecium (Ryland 1976; Todd 1978, 1979; Chadwick and Thorpe 1981; Todd 1981). Thus, it is possible to assess Onchidoris feeding by measuring polypide mortality.
Specimen collection and maintenance
Onchidoris was collected from rocks in the low-intertidal zone of Bailey Island, ME (N 43.718, W 70.002). Electra and Membranipora were collected growing on Chondrus crispus and Fucus vesiculosus respectively at sites on Bailey Island. The nudibranchs and bryozoans were brought back to the Bowdoin College Coastal Studies Center Marine Lab and maintained in running seawater at approximately ambient field temperature (8–12°C for long-term experiments, 15–16°C for video predation observations). Nudibranchs were provided a diet of both bryozoan species, but they were starved for 1–3 d prior to experiments.
Long term experiment
Chambers were incubated in a flow-through seawater tank at ambient environmental temperature (8–12°C)(Fig. 1B). Zooid status was recorded at the beginning (day 0), middle (day 4), and end (day 11) of the experiment using a digital camera (Nikon CoolPix 995) and imaging software (Image J). To maximize the likelihood that the nudibranch would discover potential prey, individual Onchidoris were placed on the rectangles in the treatments involving only one option, or the nudibranch was placed between the rectangles in the choice treatments. On day 4 of the experiment, substantial predation had occurred in at least some of the treatments. At that time, we recorded the presence or absence of the nudibranch on each type of substratum for all treatments, and we recorded zooid status for bryozoan colony treatments with nudibranchs. Treatments were replaced and allowed to incubate for a subsequent 7 days, when all colonies were imaged and presence-absence observations for nudibranchs again recorded.
Each zooid in each colony piece was counted and classified (Cell Counter plugin, Image J). Zooids were categorized as either: (1) empty, (2) polypide (containing an intact membrane and full polypide), (3) brown body, or (4) bud (small brown body and partial polypide). Counts included only intact zooids (zooecium intact). Image J was also used to measure nudibranch length.
Video predation observations
Because the bryozoans had been fed a bright red phytoplankton (Rhodomonas sp.) before filming, each polypide that had been actively feeding was bright red, which made it easier to see when the slug ate a polypide. The time it took to eat at least 20 individual polypides was recorded from each video. Since it is a suctorial feeder, Onchidoris spends much of its time feeling around for the opening into the zooid (Ryland 1976). We observed that slugs sometimes began eating one polypide, but moved on to another one before coming back to finish off the first. The time it took for the slugs to move back and forth among polypides and eat a number of them at once was recorded but categorized separately from instances where the slug concentrated on eating one entire polypide at a time.
Long term experiment
Consumption rate was measured as the number of polypides consumed per hour. To test which species of bryozoan Onchidoris could consume faster, we used a repeated measures ANOVA (Proc GLM, SAS v. 8.02) to compare consumption rates, using bryozoan species (Membranipora or Electra) as the fixed factor and time period (days 0–4 vs. days 4–11) as the repeated measure. Only treatments with no choice between bryozoans were included in this analysis of consumption rate.
To test whether Onchidoris prefers one bryozoan species over the other, we again compared consumption rates with bryozoan species (Membranipora or Electra) as the fixed factor and time period (days 0–4 vs. days 4–11) as the repeated measure. We also included a random nudibranch factor to account for consumption of each bryozoan species by the same nudibranch in the same container (Proc Mixed, SAS v. 8.02). Only treatments where the nudibranch was offered a choice between bryozoans were included in this analysis.
Video predation observations
An unpaired t-test (Proc TTEST, SAS 8.02) was used to measure the difference in consumption rate between bryozoan species when the slug was eating one polypide at a time and a separate t-test was performed for when the slugs ate two polypides at one time. A t-test was also performed to determine whether there was a difference between bryozoan species in the number of polypides that the slugs ate at a time.
Does the algal substratum affect the behavior of Onchidoris?
Onchidoris was found on Electra in one quarter of the bryozoan treatments (8 out of a total of 32), and on Membranipora in one eighth (4 out of 32). As seen in other studies (Chadwick and Thorpe 1981), Onchidoris showed no attraction to either algal substratum and was never found on the bare algae. Thus, we assumed that the different algal substrata did not affect the slugs’ behavior.
Does Onchidoris readily consume both bryozoan species?
Does Onchidoris eat Electra and Membranipora at different rates?
Long term experiment
Video predation observations
Does Onchidoris prefer to eat Electra or Membranipora when given a choice?
Feeding rate variation
In this study, average Onchidoris feeding rates measured over many days ranged from 0.13–0.66 polypides h−1 and 0.09–0.82 polypides h−1 on Electra and Membranipora respectively. These values are at the lower end of the published range. However, feeding rates for Onchidoris vary widely. Published rates include 0.4–5.2 polypides h−1 (Todd 1981), 2–12 polypides h−1 (Havenhand and Todd 1988), and 3–30 polypides h−1 (Todd and Havenhand 1989) for feeding on Electra, and 0.1–1.25 polypides h−1 for feeding on Membranipora (Chadwick and Thorpe 1981). Onchidoris consumption rates can depend on size, but size does not have as large an effect for larger slugs (Todd and Havenhand 1989), and the slugs used in this study (mean ± SD: 6.8 ± 0.2 mm and 6.4 ± 0.3 mm in the long-term study and video observations respectively) are relatively large as Onchidoris rarely gets longer than 10mm (Havenhand and Todd 1988).
Another source of variation in feeding rates is that Onchidoris does not eat constantly (Chadwick and Thorpe 1981; Todd and Havenhand 1989). Feeding rates are inconsistent primarily because of the variation in time spent eating, while the zooid handling time is presumed to be less variable (Todd and Havenhand 1989). When watching Onchidoris eating on time-lapsed video recordings, we found that mean consumption rate (based on the time it took to eat a single polypide) was much higher when the slug was eating Membranipora (34.8 ± 2.4 polypides h−1) than Electra (21.6 ± 1.8 polypides h−1). However, we also found that Onchidoris tends to concentrate on eating more than one Electra polypide at a time, but generally concentrates on eating only one Membranipora polypide at a time. Although handling time of Membranipora polypides is lower, the total consumption by the slugs is strongly affected by the amount of time spent eating. Variation in the amount of time spent eating can help explain some of our results. When Onchidoris was not given a choice, it ate more Membranipora than Electra in the first four days of the experiment, but ate more Electra in the next seven days. The slugs must have spent more time eating Membranipora in the first four days, but spent more time eating Electra in the next seven days. What caused this variation in time spent eating remains unclear.
Nudibranch feeding preference
When given a choice, Onchidoris eats more Electra than Membranipora. When not given a choice, Onchidoris can eat Membranipora faster, but it does not always spend as much time feeding on Membranipora.
If we divide the colony area (50 mm2) by the total number of zooids in the colony, we can get an average zooid size for each species. Membranipora zooids were 0.21 ± 0.03 mm2 (mean ± SD), while Electra zooids were 0.15 ± 0.02 mm2 in area. Given that Membranipora zooids are larger and they can be consumed faster, it would seem more beneficial for Onchidoris to consume Membranipora. However, Onchidoris may prefer Electra polypides because they are of higher nutritional quality. In addition, Electra is found in what may be a more suitable microhabitat for Onchidoris. Electra is very abundant on a red turfy algae, Chondruscrispus, where Membranipora is not found (Berman et al. 1992; M.C. Pratt, personal observation). Onchidoris may be better protected from dislodgement and/or predators when it is in the C. crispus canopy making it a better species of seaweed to forage on. In addition, Electra covering C. crispus has higher winter survival than Membranipora does on other seaweeds (M.C. Pratt, personal observation), so perhaps Electra is simply a more reliable food source over the winter.
This study is limited in scope to looking at the feeding preference of Onchidoris when only exposed to two species of bryozoans. In the field in Maine, Onchidoris has other food choices beyond Membranipora and Electra such as Celleporella hyalina (Chadwick and Thorpe 1981; Todd 1981; personal observation). While bryozoan and nudibranch densities have not yet been measured in the field, local sites on Bailey Island, ME where this study took place tend to have algae dominated by Membranipora and Electra (personal observations). To have a more complete understanding of food preference and the consequences of such preferences, further studies are needed to measure what bryozoan species Onchidoris is eating in the field, how much time it spends eating each species, as well as the abundance of Onchidoris relative to its food supply.
Implications of the Membranipora invasion on the community
Onchidoris has an annual life cycle. The slugs typically reproduce in the spring, and the larvae settle in the summer and early fall. The slugs then eat and grow in the fall and winter and cease feeding in the spring when they start reproducing (Todd 1978, 1987; Bleakney 1996). Contrary to the timing of this typical life cycle, Onchidoris has been seen laying eggs on top of Membranipora colonies in the winter at the Isle of Shoals (Harris and Matheison 2000). Is Onchidoris shifting its life cycle to take advantage of the huge supply of Membranipora in the late summer and early fall? Continued monitoring of the life cycle of Onchidoris will reveal any shifts that result from the Membranipora invasion.
Regardless of whether or not Onchidoris prefers Membranipora over Electra, as long as the slug eats Membranipora there may be consequences for the entire community. If enough Onchidoris slugs eat Membranipora, the Membranipora population may be kept from dominating the epibiont community. In addition, the Onchidoris population could increase substantially by taking advantage of the very large seasonal food supply of Membranipora. If Onchidoris still prefers Electra, a larger Onchidoris population could have a substantial negative effect on the Electra population. Alternatively, Onchidoris may not eat much Membranipora, thus allowing Membranipora to continue to dominate the epibiont community.
When both species of bryozoans settle on an algal host, Membranipora tends to overgrow Electra and dominate the alga (Berman et al. 1992; M.C. Pratt, personal observation). Thus, Membranipora may effectively exclude Electra from certain algal hosts such as kelps where Membranipora dominates, and algae such as C. crispus could be a refuge from competition for Electra. However, because Onchidoris prefers C. crispus microhabitats, C. crispus would not be a refuge from predation.
The effect of Onchidoris on Membranipora and vice versa will depend on feeding preference as well as other factors such as water flow. Since Onchidoris does eat other bryozoan species and even prefers other species such as Electra, this slug may not have a large impact on the Membranipora population when alternative prey is available. In addition, what microhabitat Onchidoris spends most of its time in will also have an effect on what it eats. In high flow environments, the slugs might prefer microhabitats with a reduced risk of dislodgement such as C. crispus. Onchidoris may not have a large impact on Membranipora in high flow environment because Membranipora is found more often growing on kelps and fucoids where dislodgement risk may be higher. Since many factors can influence the effect of Onchidoris on Membranipora and vice versa, there may only be certain circumstances when predation does reduce the Membranipora population such as when there are fewer alternative prey species available and water velocity is slower. Further research is needed in the field to see how factors such as alternative prey and flow velocity affect the impact of Onchidoris on Membranipora.
Our observations in the field on Bailey Island, Maine do not suggest that predation is currently having a significant effect on the Membranipora population (M.C. Pratt, personal observation), and observers in Atlantic Canada have similarly seen little effect of Onchidoris on Membranipora (Chapman et al. 2002). However, this system appears to be dynamic, as suggested by observations further south where a substantial number of Onchidoris slugs have been seen on Membranipora (Harris and Matheison 2000). Future research should include following the populations of these species and their interactions in the field to determine how the Membranipora invasion will affect the Onchidoris population and vice versa in the long term. While the introduction of non-native species can have substantial negative effects, such introductions can also provide the opportunity to observe the evolution of biological interactions such as predation and competition (Lodge 1993; Casey 2005). Thus, it is important to measure the interactions of invasive species with other organisms in their new habitats over long time scales so we can learn how such interactions evolve.
We thank the Bowdoin College Coastal Studies Center for use of space at the Marine Lab. M. Pizer and anonymous reviewers provided comments that helped improve this paper substantially.
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