Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions

Abstract

The spread of exotic species and climate change are among the most serious global environmental threats. Each independently causes considerable ecological damage, yet few data are available to assess whether changing climate might facilitate invasions by favoring introduced over native species. Here, we compare our long-term record of weekly sessile marine invertebrate recruitment with interannual variation in water temperature to assess the likely effect of climate change on the success and spread of introduced species. For the three most abundant introduced species of ascidian (sea squirt), the timing of the initiation of recruitment was strongly negatively correlated with winter water temperature, indicating that invaders arrived earlier in the season in years with warmer winters. Total recruitment of introduced species during the following summer also was positively correlated with winter water temperature. In contrast, the magnitude of native ascidian recruitment was negatively correlated with winter temperature (more recruitment in colder years) and the timing of native recruitment was unaffected. In manipulative laboratory experiments, two introduced compound ascidians grew faster than a native species, but only at temperatures near the maximum observed in summer. These data suggest that the greatest effects of climate change on biotic communities may be due to changing maximum and minimum temperatures rather than annual means. By giving introduced species an earlier start, and increasing the magnitude of their growth and recruitment relative to natives, global warming may facilitate a shift to dominance by nonnative species, accelerating the homogenization of the global biota.

Fig. 1.

(a) Annual mean winter (January 1–March 31) water temperature (°C) for 1976–2001 at Millstone, CT. The dashed box indicates the time period for which recruitment data have been collected at Avery Point. Least-squares regression was used for curve fitting. Slope = 0.07, P < 0.01, R² = 0.24. (b–d) March 1 water temperature is strongly negatively correlated with the timing of the onset of recruitment for three nonnative ascidians, B. violaceous, D. listerianum, and A. aspersa. The vertical axis is the number of days since the beginning of the calendar year (i.e., day 181 = July 1). For each of these nonnative species, recruitment begins earlier in years with warmer winters. Native ascidians showed no correlations between timing of onset of recruitment and interannual variation in water temperature. For analysis, see Table 1.

Fig. 2.

Total annual recruitment of introduced (nonnative) species is positively correlated with mean water temperature during the preceding winter (Jan 1–March 31), whereas native species recruitment is negatively correlated with winter temperatures. Total recruitment data were log-transformed to meet assumptions of ANCOVA. ANCOVA results: temperature F = 0.94, P = 0.348; native status F = 11.99, P = 0.003; temperature⋅status F = 11.57, P = 0.004. Parameter estimates of linear curve fits: Nonnatives: slope = 0.28, P = 0.007, R² = 0.49, slope P = 0.007; natives: slope = −0.15, P = 0.108, R² = 0.32.

Fig. 3.

Native (Botryllus) and introduced (Botrylloides, Diplosoma) ascidians show similar growth rates at moderate temperature, but at higher temperatures the nonnative species have greater growth rates than an ecologically similar native. ANOVA results: 16.1–19.0°C: F = 0.96, P = 0.39; 19.1–21.0°C: F = 7.9, P = 0.0006; 21.1–23.3°C: F = 42.7, P < 0.0001. ANOVA was not done for 14.5–16.0°C because of poor replication for Botrylloides; unpaired t test indicated that growth of Botryllus and Diplosoma did not differ at this temperature (df = 29; P = 0.14). Different letters above each bar indicate significant differences in growth among species within that temperature range by using Tukey–Kramer post hoc tests at P < 0.05.