Biological control of aquarium pest anemone Aiptasia pallida verrill by peppermint shrimp Lysmata risso.

ABSTRACT Caridean shrimp in the genus Lysmara Risso are widely traded in the aquarium hobby industry. Peppermint shrimp Lysmata spp. have been used to control the brown (glass) anemone, Aiptasia pallida Verrill, a significant pest in the aquarium environment. A study was conducted to quantify the ability of two peppermint shrimp in controlling A. pallida, Lysmata Sp. (Haiti variety) tended to have a higher consumption rate of sea anemone than Lysmata sp. (Florida Gulf Coast variety). Shrimp in a group tended to have a lower consumption rate per shrimp than individual shrimp in both species, but were capable of preying upon larger anemones. Larger (euhermaphrodite-phase) Lysmata (Florida Gulf Coast variety) had a higher rate of sea anemone consumption than that of smaller (male-phase) shrimp.

KEY WORDS: Aiptasia pallida, anemone, Lysmata, peppermint shrimp, predation 

INTRODUCTION

Species of caridean shrimp Lysmata are commonly traded in the marine aquarium industry due to their striking coloration, beneficial symbiotic relationships, and quick acclimation to a captive environment. Many Lysmata species also teed on parasites of fish (Van Tassel et al. 1994; but see Spotte 1998), and therefore play an important role in the natural and aquarium environments.

The cleaner shrimps L. amboinensis De Mann, L. grabhami Gordon. and L. debelius Bruce are revered for their ability to clean fish and their brilliant coloration, therefore command a high market price. Peppermint shrimp, several species of Lysmata with red or maroon stripes along the entire length of their translucent bodies, are not as brightly colored. However, they are in high demand for their apparent ability to control the common marine aquarium pest anemone Aiptasia pallida. Though the unit price is much less than that of L. amboinensis, L. grabhami, and L. debelius, the total volume sold annually greatly exceeds that of any other shrimp in the marine aquarium industry. Although peppermint shrimp are marketed under the name L. wurdemanni Gibbes, the vast majority of shrimp sold are in fact a novel species misidentified as L. rathbunae Chace (Rhyne 2002, Rhyne & Lin, in preparation). There are clear morphologic and some distribution differences, evidences of reproductive incompatibility and species-level genetic differences in the group. This confusion has resulted in unreliable reports of the most effective species for controlling A. pallida. Another unique feature of Lysmata species is their reproductive system, protandric simultaneous hermaphroditism (Bauer 2000), in which shrimp first mature as males and then change to simultaneous hermaphrodites. A proportion of the shrimp, influenced by group size, may remain as males (Lin & Zhang 2001).

Brown (glass) anemone Aiptasia pallida (Aiptasiidae) is a common pest in marine aquariums. They are commonly found in shallow and nutrient-rich waters along the subtropical and tropical Atlantic coasts. The brown color is caused by a unicellular symbiotic zooxanthaelle, Symbiodinium microadriaticum Freudenthal, which allows the anemone to thrive in highly illuminated environments (Trench 1993), including the marine reef aquariums. Aiplasia rapidly reproduce asexually by pedal laceration (budding from their pedal disc) (Hunter 1984). When it occurs in dark places, A. pallida is not brown due to loss of zooxanthaelle, but rather a pure pallod white, hence the second half of its Latin name.

Slinging nematocysts within the anemone tentacles contain the venom beta phospholipase A2 and are used to stun prey or defend against potential predators (Grotendorst & Hessinger 2000). In the aquarium, these anemones harm both soft and hard corals and other sessile invertebrates, causing irritation and eventual death. The transparency and cryptic nature of Aiptasia results in its regular introduction into the marine aquarium from live rock or corals. Aiptasia cannot be eliminated by regular cleaning of aquarium. Many aquarium owners attempt to crush the anemones, which often promotes their proliferation and colonization in other areas of the tank. Aiptasia is commonly eliminated chemically and biologically. Chemical elimination is effective, but requires the laborious introduction of toxic injections directly into the oral disc of each anemone. Biologic control via anemone's natural predators eliminates the use of toxins. The nudibranch Berghia verrucicornis Costa (e.g., Carroll & Kempf 1990), butterflyfish (Chelmon rostratus Linnaeus and Chaetodon kleini Bloch), and peppermint shrimp are commonly used as successful natural predators of Aiptasia. However, there is no scientific study to quantify the effectiveness of such control.

The purpose of this study is to document the predation of two peppermint shrimp species, Lysmata sp. (Haiti variety) and Lysmata sp. (Florida Gulf Coast variety) on A. pallida. Though both shrimp are novel species, they are both commonly traded as L. wurdemanni Gibbes.

MATERIALS AND METHODS

The experiments were conducted at the Aquaculture Laboratory, Florida Institute of Technology, in 2002. Aiptasia pallida specimens were obtained from a local aquarium store and cultured in a 40-L tank. Anemones were fed live Artemia nauplii under constant light for 60 days and allowed to asexually reproduce on the glass walls of the aquarium. A razor blade was used to gently scrape the pedal disc base of the anemones, and the anemones were then placed on the rough surfaces of ceramic tiles. Each tile (11 x 11 cm) was carefully placed in a 10-L aquarium, and anemones were allowed to adhere to the tiles for a minimum of 24 h. Location of anemones on the tiles was haphazard due to the natural movement of anemones during reattachment.

Two species of peppermint shrimp, Lysmata sp. (Florida Gulf Coast variety) (collected from north of Tampa Bay) and Lysmata sp. (Haiti variety, collected from Haiti) were tested as anemone predators. The Florida Gulf Coast variety used in the current study was referred to as "L. wurdemanni" in some past studies (Zhang et al. 1998a, Zhang et al. 1998b). These shrimp do not conform to any current species definition, but are popularly (and mistakenly) referred to as L. rathbunae (see Debelius 2001 for photographs). We will refer to this species as Lysmata (gulf) in this paper. The Haiti variety was incorrectly recorded as L. wurdemanni by Holthuis (1959) and was referred to as such by Lin and Zhang (2001), and will be referred to as Lysmata (Haiti). This shrimp has pink gonads and a carmine red transverse stripe on the third abdominal segment, whereas Lysmata (gulf) has green gonads, a dark crimson telson, and does not have a transverse pigment stripe on the third abdominal segment. Both novel species tested are currently being described as part of a review of the peppermint complex found in the Western Atlantic (Rhyne and Lin, in preparation).

Test shrimp were maintained in a recirculating system. Each shrimp was placed into a marked container and fed frozen adult Artemia once daily in the afternoon after anemone feeding trials. Salinity and temperature were maintained at 35 and 26[degrees]C, respectively, for all the experiments.

To compare the consumption rates of the sea anemones (5-10 mm in oral disc diameter) by the two shrimp species, nine replicate shrimp of Lysmata (gulf) and Lysmata (Haiti), respectively, that had not previously fed on Aiptasia were used. Total length (TL) of each shrimp was measured. A single shrimp was placed into an enclosure within a 10-L aquarium that contained a tile with 9 to 11 anemones and allowed to acclimate for 15 min before being released into the aquarium. The time between release and each feeding and total number of anemones consumed were recorded. The shrimp was observed until all the anemones were eaten or for 24 h. An additional experiment was conducted to examine the feeding rate and behavior if multiple shrimp were present in an aquarium. Four groups (two for each species) of five shrimp of similar sizes were used. Each group was placed in a 10-L aquarium with a tile of 10 anemones. Again, the shrimp were confined to a holding pen and allowed to acclimate for 15 min prior to being released. The time from the shrimp's release to each feeding was recorded. The shrimp was allowed to feed until all the anemones were consumed.

To test the effect of shrimp size on its ability to feed on sea anemones, six large euhermaphrodite-phase and eight small male-phase Lysmata (gulf) were introduced individually into a 10-L aquarium with sea anemones 15-10 mm oral disk diameter) attached on a single tile. There was an average ([+ or -] SD) of 14.8 ([+ or -] 2.2) and 9.6 ([+ or -] 3.1) anemones for each large and small shrimp, respectively. Each shrimp was confined to a holding pen and allowed to acclimate to the test aquarium conditions for 15 min prior to release. The number of sea anemone consumed was recorded after 24 h.

RESULTS

The average (SD) TL of Lysmata (gulf) and Lysmata (Haiti) was 24.1 (4.0) and 23.3 (5.2) mm, respectively. One shrimp of each species did not consume any anemone in 24 h. Excluding these two nonfeeding shrimp, an average (SD) of 9.1 (0.8) anemones was consumed by Lysmata (Haiti) in an average (SD) of 73.1 (26.8) min; and an average (SD) of 6.1 (2.4) anemones was consumed by Lysmata (gulf) in an average (SD) of 129.3 (78.9) min. The average ([+ or -] SD) consumption rate of Lysmata (Haiti) (10.1 [+ or -] 9.5 per h) is not significantly higher than that of Lysmata (gulf) (6.8 [+ or -] 12.1 per h), due to large variations. The large variation in each species is due to one "outlier." If the "outlier" is removed from each species, the average ([+ or -] SD) consumption rate of Lysmata (Haiti) (6.8 [+ or -] 1.6) is significantly (t test, P < 0.05) higher than that of Lysmata (gulf) (2.5 [+ or -] 1.3). Lysmata (gulf) also had a significantly (t test, P < 0.05) longer, average ([+ or -] SD) response time (10.9 [+ or -] 10.4 min) (from release to first feeding) than that of Lysmata (Haiti) (2.3 [+ or -] 3.7 min).

The average (SD) TL of the first group of Lysmata (Haiti) was 18.0 (2.1) mm and it took the shrimp 48 min to consume the 10 anemones. The average (SD) TL of the second group of Lysmata (Haiti) was 19.0 (2.2) mm, and it took the shrimp 78 min to finish the 10 anemones. For Lysmata (gulf), the average (SD) TL of the first group was 22.0 (2.1) mm, and it took the shrimp 90 min to consume the 10 anemones. The average (SD) TL of the second group was 20.5 (4.1) mm, and it took the shrimp 31 min to consume the 10 anemones.

Large individuals (average [+ or -] SD, TL = 41.0 [+ or -] 3.0 mm) of Lysmata (gulf) consumed an average (SD) of 12.8 (4.3) anemones [out of 14.8 (2.2) offered] in 24 h, significantly (t test, P < 0.05) higher than that consumed [5.4 (4.3) anemones out off 9.6 (3.1) offered] by the small shrimp (average [+ or -] SD, TL = 19.9 [+ or -] 1.6 mm) during the same time period.

DISCUSSION

Both Lysmata species are capable of controlling Aiptasia pallida. Lysmata (Haiti) tended to have a higher predation rate and shorter response time than Lysmata (gulf). In Lysmata (gulf) at least, larger (euhermaphrodite phase) shrimp consumed more anemones than smaller (male-phase) shrimp. Shrimp in a group tended to have a lower consumption rate per shrimp than individual shrimp. This may be a result of social interactions among the shrimp. Group feeding was not observed as cooperative, but competitive. In most cases, only one shrimp in a group was observed feeding on a small anemone at a time. However, a group of shrimp would feed on large anemones together and were able to consume larger anemones than an individual shrimp (unpublished data). Group feeding appeared to be cooperative for feeding on large anemones and competitive for feeding on small ones.

When attacking anemones, shrimp were prone to be stung with nematocysts and usually chose smaller, less harmful anemones. Peppermint shrimp appear to locate randomly the first anemone. Alter consuming the first anemone, the shrimp were observed readily seeking out other prey. The consumption of the first anemone appeared to invoke a feeding response. A shrimp would normally repeatedly approach the anemone until the anemone withdrew its tentacles. Then the shrimp would begin to consume voraciously the anemone. Some shrimp were observed making predation attempts, but were never successful. These shrimp may have molted recently, and their exoskeleton may be more sensitive to nematocysts (personal observation).

We observed that even satiated shrimp (after being fed with Artemia nauplii for an hour) would attempt to attack the anemones, but rescinded after being stung by the nematocysts. After a period of 24 h, the shrimp would successfully prey on anemones. While this study does not address the ability of shrimp to eat anemones over 10 mm oral disc diameter, both large shrimp (>3 cm TL) and groups of three to five shrimp have been observed to consume large (20 mm oral disc diameter) anemones (unpublished data).

ACKNOWLEDGMENTS

The authors thank Brandi Sloss and Vanessa Maxwell for assistance in the laboratory.

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ANDREW L. RHYNE *, JUNDA LIN, AND KATHIE J. DEAL ** Department of Biological Sciences, Florida Institute of Technology, Melbourne, Florida 32901

* Corresponding author. E-mail: [e-mail]

** Present address: Department of Marine and Environmental Systems, Florida Institute of Technology, Melbourne, Florida 32901.