Marine Biology (2005) 147: 225–234 DOI 10.1007/s00227-004-1539-8
R ES E AR C H A RT I C L E
Xiping Ma Æ J. E. Purcell
Temperature, salinity, and prey effects on polyp versus medusa bud production by the invasive hydrozoan Moerisia lyonsi
Received: 4 March 2004 / Accepted: 19 November 2004 / Published online: 10 March 2005 Springer-Verlag 2005
Abstract Hydrozoan species are renowned for flexible asexual reproduction, which may predispose them to be successful invaders. Polyps of the invasive hydrozoan Moerisia lyonsi (Boulenger, 1908) have very high rates of asexual production of both polyp and medusa buds. In order to determine how environmental factors affect asexual reproduction in M. lyonsi, the quantitative relationships between polyp bud and medusa bud production were studied in a 31-day laboratory experiment during August 2001. The combined effects of prey (4, 8, 12, 16 Acartia tonsa copepods polyp 1 day 1), temperature (20C, 29C), and salinity (5, 15, 25) were tested on the development times for polyp buds (DTp) and medusa buds (DTm), the total asexual reproduction rate (ARR, no. buds polyp–1 day–1), and the ratio of medusa bud to total bud production (Rm). Greater food consumption significantly and directly enhanced ARR and Rm and shortened DTp and DTm. A lower temperature (20C) and higher salinity (25) reduced food consumption, lengthened development times, and decreased ARR and Rm, with opposite effects for the higher temperature (29C) and lowest salinity (5). The patterns of variation of these reproductive parameters are more complex. DTm was most sensitive and was significantly and directly affected by all three measured factors. In addition to food consumption, direct effects were seen by temperature on DTp and by salinity on Rm. ARR was directly affected only by food consumption. Overall, DTp, DTm, and
Communicated by J.P. Grassle, New Brunswick X. Ma Æ J. E. Purcell (&) University of Maryland Center for Environmental Science, Horn Point Laboratory, Cambridge, MD 21613, USA E-mail:
[email protected] Fax: +1-360-2931083 Present address: J. E. Purcell Western Washington University, Shannon Point Marine Center, Anacortes, WA 98221, USA
Rm were more sensitive to environmental differences than was ARR. More favorable conditions enhanced medusa bud production. The adaptive reproductive processes and their significance for the maintenance and dispersal of M. lyonsi are discussed.
Introduction Hydroid species display a wide variety of life cycles and reproductive processes (reviewed by Shosta 1993; Fautin 2002). For example, some species, such as freshwater hydras, do not have a pelagic medusa stage; some, such as trachyline medusae, do not have a benthic polypoid stage; some have both stages; some hydroids externally brood polyp and/or medusa buds; some spawn gametes; and others possess still different reproductive methods (Boero 1984; Madin and Madin 1991; Shosta 1993; Fautin 2002). Many species of hydromedusae, such as Moerisia lyonsi, have both a sexual pelagic medusa phase and an asexually budding, colonial, benthic polyp (hydroid) phase in their life cycle (Fig. 1). Vigorous asexual reproduction contributes to the establishment of the invasive hydrozoan M. lyonsi (in Purcell et al. 1999a; Ma and Purcell 2005), which probably originated from the Black Sea or Middle East regions, in several estuaries around the US coastline (Calder and Burrell 1967; Calder 1971; Sandifer et al. 1974; Poirrier and Mulino 1977; Dumont 1994). Reproduction in M. lyonsi is characterized by high rates of asexual reproduction of both planktonic (medusa) and non-planktonic (polyp) buds, short development time, and dioecious medusae (Purcell et al. 1999a). Polyps of M. lyonsi asexually produce polyps, both on the stolon and as buds on the hydranth, and medusae, as well as forming dormant cysts. In favorable conditions, a polyp bud begins budding within 2–3 days after detaching from its founder polyp, with polyp buds
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Materials and methods
Fig. 1 Moerisia lyonsi. Life history
produced first and medusa buds produced later (Purcell et al. 1999a). The most favorable conditions, in which the most polyp and medusa buds were produced, were 29C and salinities of 5–20 when tested in 45 combinations of temperature (10–29C) and salinity (1–40) (Ma and Purcell 2005). The free-swimming medusa of M. lyonsi is transparent and usually 2 weeks longer at 20C than at 29C. Therefore, the significantly longer time between DTp and DTm at 20C than at 29C (Fig. 2) was caused mainly by a delay in medusa bud production. In addition, the between-salinity difference was also much greater for DTm than for DTp (Fig. 2). The detrimental effects of high salinity (25) to DTm were more obvious at 20C than at 29C (Fig. 2). At 20C and 25 salinity, most of the treatments never produced medusa buds in 34 days, regardless of food consumption (Fig. 2A). The results of ANCOVA tests on DTp and DTm (Table 2) generally agreed with the above observations (Fig. 2). Temperature and food consumption both had significant effects on DTp and DTm, whereas salinity had significant effects on DTm, but not on DTp. Food consumption (F) was negatively and linearly related to both DTp and DTm. The effects of F on DTp were similar at different temperatures and salinities (F · T, F · S). By contrast, the effects of F on DTm were similar at different temperatures, but different at different salinities (F · T, F · S). The least square means (LSM) for both DTp and DTm were significantly shorter at 29C than at 20C (P34 >34 29.7±3.8 >34 10.3±1.2 9.0±0 8.7±0.6 8.0±0 11.0±1.0 11.3±2.1 9.7±0.6 8.7±1.2 20.7±6.4 12.7±1.2 12.0±0 11.0±1.0
1.26±0.18 1.98±0.19 2.42±0.09 3.18±0.41 1.61±0.07 2.25±0.18 3.44±0.30 4.21±0.05 0.67±0.13 1.10±0.14 1.67±0.15 1.95±0.26 0.97±0.03 1.99±0.43 3.01±0.93 4.75±0.80 1.30±0.19 2.83±0.26 3.70±1.02 5.95±0.22 0.50±0.41 1.12±0.41 1.57±0.53 2.56±0.16
0.27±0.15 0.23±0.08 0.41±0.06 0.27±0.06 0.11±0.05 0.25±0.02 0.24±0.07 0.19±0.06 0 0 0.01±0.02 0 0.34±0.26 0.63±0.11 0.59±0.08 0.74±0.04 0.36±0.11 0.29±0.21 0.33±0.16 0.70±0.08 0.14±0.11 0.29±0.11 0.24±0.11 0.62±0.08
15
25
29
5
15
25
be significant because the degree of freedom for temperature was only 1. Because of the dependence of F on temperature and salinity, the interpretations of ANCOVA results will be somewhat different. For example, the results of the ANCOVA test described in the previous paragraph (Table 2) showed that F had significant effects on DTp, while salinity did not, but after incorporating the F dependence on salinity, the result means that salinity had indirect effects on DTp by affecting food consumption of the polyps. Total asexual reproduction of M. lyonsi polyps in 31 days (ARR) increased linearly with increasing food consumption (F) in all temperature and salinity treatments (Fig. 3). ANCOVA results showed that food
consumption had significant direct effects on ARR, but neither temperature nor salinity had significant direct effects on ARR (Table 4). Hence, food consumption was an essential factor in controlling the total asexual reproduction. However, due to the significant dependence of F on temperature and salinity, the ANCOVA result really means that temperature and salinity affected ARR indirectly by affecting food consumption by the polyps. Additionally, the slopes in which ARR increased with increasing food consumption were statistically different among temperatures (F · T) and salinities (F · S) (Table 4). The ratio of medusa bud production to the total asexual reproduction (Rm) was very sensitive to the
Table 2 Moerisia lyonsi. Statistical results of ANCOVA tests on the effects of temperature (T) and salinity (S) on development time of polyp buds (DTp) and of medusa buds (DTm), with food consumption (F, copepods polyp–1 day–1) as a covariate (df degrees of
freedom; MS mean square in type III ANOVA table). The df-value for DTp marked by asterisk is due to deletion of one abnormal data point.F-values marked by asterisks were computed using the error term for T·S to better fit the experimental design
Source
Model Error T S F T·S F·T F·S T·S·F
DTp
DTm
df
MS
F-value
P
df
MS
F-value
P
11 59* 1 2 1 2 1 2 2
17.05 1.07 8.34 1.25 6.70 0.29 1.51 0.08 0.06
15.88
