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‡Rhode Island Hospital and Brown Medical School, Rhode Island 02903, USA §Department of Neurology, Children’s Hospital, Boston, Massachusetts 02115, USA 1. Patrick, G. N. et al. Nature 402, 615–622 (1999).

2. Lee, K. Y. et al. Neurosci. Res. 34, 21–29 (1999).

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135–147 (2001).

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Nixon, R. Brain Res. 763, 145–158 (1997).

Ecosystems

Reef corals bleach to survive change

T he bleaching of coral reefs, in which symbiotic algae are lost from reef- building invertebrates, is usually con-

sidered to be a drastic and damaging response to adverse environmental condi- tions1,2. Here I report results from trans- plant experiments involving different combinations of coral host and algal symbiont that support an alternative view, in which bleaching offers a high-risk ecological opportunity for reef corals to rid themselves rapidly of suboptimal algae and to acquire new partners. This strategy could be an advantage to coral reefs that face increasingly frequent and severe episodes of mass bleaching as a result of projected climate change2,3.

Coral reefs are built by symbioses between scleractinian (stony) corals and photosynthetic dinoflagellate algae. These diverse algae4 are important species because their loss during bleaching can lead to widespread coral mortality and degradation of reef ecosystems5. Different types of algal symbiont often show strong zonal patterns within their coral hosts that correspond to light intensity (shallow, ‘high-light’ algae or deep, ‘low-light’ algae)6–8.

To investigate the effect of bleaching on the stability of these depth distributions, I reciprocally transplanted eight species of Caribbean scleractinian coral between ‘shallow’ (2–4 m) and ‘deep’ (20–23 m) sites in the San Blas archipelago, Panamá. I assessed transplanted and control colonies for bleaching after 8 weeks, and for mortali- ty and changes in symbiont taxa after 12 months (Fig. 1).

‘Upward’ (deep-to-shallow) transplants showed significant bleaching after 8 weeks (11 of 24 colonies partially or severely bleached; 2 others pale), whereas ‘down- ward’ (shallow-to-deep) transplants showed less bleaching (0 of 37 colonies bleached; x2420.7, Fisher’s exact P*0.0001). Surpris- ingly, despite more extensive bleaching, upward transplants showed no mortality after 12 months (0 of 24 colonies dead), unlike downward transplants (7 of 37 colonies dead; x245.13, Fisher’s exact P40.0358). Control transplants showed no

significant bleaching or mortality. Changes in the structure of symbiont

communities explained these surprising patterns of bleaching and mortality. Sur- veys of restriction-fragment-length poly- morphisms in genes encoding large-subunit ribosomal RNA4,8 identified four groups of Symbiodinium algae (termed A, B, C, and a previously unassigned clade, D4,8,9) from these coral hosts. Five of the eight coral host species showed strong intraspecific patterns of depth zonation in their symbionts; the other three showed no such patterns8 (Fig. 1). Transplanted coral species that hosted different algae at deep and shallow sites adjusted their algae distributions to their new depths only when transplanted upwards (12 of 16 colonies), and not when transplanted downwards (1 of 25 colonies; x2422.7, Fisher’s exact P*0.0001).

These results reveal an unexpected rela- tionship between acute stress-induced bleaching (sudden exposure to increased irradiance after upward transplantation), adaptive change in symbiont communities, and reduced coral host mortality. This contrasts with a lack of bleaching in response to chronic stress (lower sustained irradiance after downward transplanta- tion), no change in symbiont communities, and increased coral mortality. Together, these findings support the view (first pro- posed by theorists10) that coral bleaching can promote rapid response to environ- mental change by facilitating compensatory change in algal symbiont communities.

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Without bleaching, suboptimal host– symbiont combinations persist, leading eventually to significant host mortality.

Reef corals are flexible associations that can switch or shuffle symbiont com- munities in response to environmental change4,8,10,11. However, there may be costs involved, as shown by higher mortality in the five coral species that vary their algae with depth (9 of 79 colonies) than in the three species that do not (0 of 39 colonies; x244.81, Fisher’s exact P*0.0289).

Changes in symbiont communities may be slow unless existing symbionts are first removed, suggesting that established symbionts have a significant competitive home advantage over invasive (or low- abundance) symbionts. Coral bleaching can rapidly remove these symbionts, facilitating their replacement by alternative algae that are better suited to the new environmental conditions. Furthermore, the process of community change, which is facilitated by bleaching, may provide a window for unusual opportunistic symbionts to colonize hosts (and/or proliferate inside them)9,11,12, as shown by the behaviour of Symbiodinium A and D in upward-trans- plant experiments.

Symbiosis recombination may help to resolve the paradox of reef corals as environ- mentally fragile yet geologically long-lived associations13. Despite the extreme risks involved1,2, and the likely high incidence of mortality in some regions (such as that resulting from the 1997–98 El Niño14),

Figure 1 Symbiont diversity and mortality responses to bleaching in transplanted corals. Bars show symbiont community structure

(Symbiodinium clades A–D) before transplantation and 12 months after transplantation: white, A; orange, B; red, C; green, D; black,

dead. Pie charts indicate bleaching status of host colonies before transplantation and 8 weeks after transplantation: dark green, healthy;

light green, pale; orange, partial bleaching; white, severe bleaching; black, dead. Vertical axes, number of colonies; horizontal axes, coral

species. Si, Pg, Pb, Dl, Ds and Ac (white background) have strong light-related patterns of symbiont diversity; Ss, Cn and Mc (blue back-

ground) exhibit no light-related patterns of symbiont diversity. Control colonies accompanied the transplanted corals to their new location

before being returned immediately to their original depths. ND, no data: Ds and Ac were very rare at the deeper location and underwent

shallow-to-deep transplantation only (at similar depths nearby they were not uncommon and contained ‘low-light’ algae7). Diagonal

arrows indicate direction of transplantation. Si, Stephanocoenia intersepta; Pg, Porites astreoides (green); Pb, Porites astreoides (brown);

Dl, Diploria labyrinthiformis; Ds, Diploria strigosa; Ac, Acropora cervicornis; Ss, Siderastrea siderea; Cn, Colpophyllia natans;

Mc, Montastraea cavernosa.

Controls Transplants

Si Pg Pb Dl Ds Ac Ss Cn Mc

ND ND

Si Pg Pb Dl Ds Ac Ss Cn Mc

ND ND

Si Pg Pb Dl Ds Ac Ss Cn Mc

Initial

Si Pg Pb Dl Ds Ac Ss Cn Mc

ND ND

Si Pg Pb Dl Ds Ac Ss Cn Mc

D e e p

( 2 0 –2

3 m

) S

h a llo

w ( 2 –4

m )

bleaching may ultimately help reef corals to survive the recurrent and increasingly severe warming events projected by current climate models of the next half-century3. Bleaching is an ecological gamble in that it sacrifices short-term benefits for long-term advantage. This counters conventional wisdom that bleaching is detrimental from all perspectives, and supports the role of symbionts as adaptive agents10,11. Andrew C. Baker Wildlife Conservation Society, Osborn Laboratories of Marine Science, New York Aquarium, Surf Avenue at West 8th Street, Brooklyn, New York 11224, USA e-mail: [email protected] 1. Brown, B. E. Coral Reefs 16, S129–S138 (1997).

2. Glynn, P. W. Coral Reefs 12, 1–17 (1993).

3. Hoegh-Guldberg, O. Mar. Freshwat. Res. 50,

839–866 (1999).

4. Rowan, R. & Powers, D. A. Science 251, 1348–1351 (1991).

5. Glynn, P. W. & Colgan, M. W. Am. Zool. 32, 707–718 (1992).

6. Rowan, R. & Knowlton, N. Proc. Natl Acad. Sci. USA 92,

2850–2853 (1995).

7. Rowan, R., Knowlton, N., Baker, A. & Jara, J. Nature 388,

265–269 (1997).

8. Baker, A. C. The Symbiosis Ecology of Reef-Building Corals.

Thesis, Univ. Miami (1999).

9. Toller, W. W., Rowan, R. G. & Knowlton, N. Biol. Bull. Mar.

Biol. Lab. Woods Hole (in the press).

10. Buddemeier, R. W. & Fautin, D. G. Bioscience 43,

320–326 (1993).

11. Rowan, R. J. Phycol. 34, 407–417 (1998).

12. Kinzie, R. A., Takayama, M., Santos, S. R. & Coffroth, M. A.

Biol. Bull. Mar. Biol. Lab. Woods Hole 200, 51–58 (2001).

13. Buddemeier, R. W. & Smith, S. V. Am. Zool. 39, 1–9 (1999).

14. Wilkinson, C. et al. Ambio 28, 188–196 (1999).

Population control

African elephants and contraception

P rotected from hunting and provided with access to water-holes during droughts, elephant numbers can dou-

ble in a decade, severely damaging natural vegetation and the many species dependent upon it. Culling is an effective but contro- versial control strategy, so Fayrer-Hosken et al.1 have assessed the efficacy of using immunocontraception through vaccina- tion, concluding that this could be a practi- cal way of controlling elephant numbers. However, an intervention feasible in repro- ductive physiology may not be a practical way to control a population. Fayrer-Hosken et al. have not considered calculations2,3 that undermine the practicality of their method, nor alternative management strategies.

Controlling elephants in Kruger National Park, South Africa, by immuno- contraception would necessitate treatment of 2,250 cows each year over an initial period of 11 years (ref. 3). Even if individual treatments were 100% effective, the costs would be likely to exceed the total manage- ment budget of the South African national parks. The best results of Fayrer-Hosken et al. involved two of ten elephants becoming

pregnant, and that was after receiving two booster vaccinations.

The effectiveness of this method may be less than claimed. Of the control group, 89% became pregnant within a year. This seems high, exaggerating the difference between treated and control groups. Data from 813 adult cows culled in Kruger National Park between 1979 and 1994 showed that 51% (range, 36–77%) were pregnant. This is to be expected: gestation lasts 22 months and the calving interval is 44 months (ref. 2), so about 50% of a sample of cows should be pregnant. Thus, on average, females go for 22 months with- out becoming pregnant. In a random sam- ple of females monitored for 12 months, only 55% (not 89%) should therefore become pregnant.

Between 16 and 1,846 elephants of all age classes and both sexes were culled annu- ally in Kruger National Park from 1967 to 1994. We share the desire to reduce culling and have sought methods to do so. Remov- ing or sterilizing 250 subadult females each year should reduce population growth to zero2,3. Moreover, densities of greater than 0.37 elephants per square kilometre result in reduced population growth rates — probably due to reduced reproductive out- put by newly sexually matured females or to increased calving intervals2. Culling, as conducted, maintained densities at which population growth was near its maximum. Culls should be delayed for one year after counts exceed 0.37 elephants per square kilometre to allow density dependence to reduce numbers naturally2. Culls may still be necessary, but they would then be much less frequent and involve far fewer animals. Stuart L. Pimm*, Rudi J. van Aarde† *Center for Environmental Research and Conservation, Columbia University, 1200 Amsterdam Avenue, New York, New York 10027, USA e-mail: [email protected] †Conservation Ecology Research Unit, University of Pretoria, Pretoria 0002, South Africa 1. Fayrer-Hosken, R. A., Grobler, D., Van Altena, J. J.,

Bertschinger, H. J. & Kirkpatrick, J. F. Nature 407, 149 (2000).

2. van Aarde, R. J., Whyte, I. & Pimm, S. Anim. Conserv. 2,

287–294 (1999).

3. Whyte, I., van Aarde, R. J. & Pimm, S. Anim. Conserv. 1,

77–83 (1998).

Fayrer-Hosken et al. reply –– Pimm and van Aarde question the feasibility of controlling elephant numbers by immunocontracep- tion, arguing that the sterilization or removal of 250 subadult cows each year is the answer to population growth. However,

there are no known safe methods of sterilizing free-roaming African elephants. Moving 250 subadult females to another park is impractical as there are very few areas able to receive elephants from Kruger National Park without becoming confront- ed with an elephant overpopulation prob- lem of their own.

This number of subadult cows cannot be moved without disrupting the social order within their herds. Keeping them in their herds would mean that (assuming a mean herd size of 12.4, as shown in our study, and an average of 3 subadult females per herd) Kruger National Park would have to move 1,033 elephants — an unrealistic and expensive proposition. Hence the only practical way to remove 250 subadult females would be to cull them, which Pimm and van Aarde agree is an unaccept- able solution.

We have shown that immunocontracep- tion using porcine zona pellucida (pZP) works in the African elephant, although its long-term effectiveness in controlling pop- ulations is still being evaluated in South Africa. The cost and speed of field delivery have not been assessed for vaccinating large groups of elephants. However, contrary to the calculations of population modellers1,2, immunocontraception has worked in herds of wild horses and white-tailed deer3.

Preserving these magnificent creatures and their genetic contribution for the future is a common goal. On the basis of a single administration of a multiple-release pZP vaccine that is being developed for use in horses (I. K. M. Liu, personal communi- cation), it should be possible to reduce the first three vaccinations used in our original study to a single dose and so minimize the stress, cost and labour of elephant immunocontraception.

We therefore question Pimm and van Aarde’s criticism regarding the practicality of field immunocontraception for Kruger Park’s elephant herds. It is our judgement that preserving these animals through immunocontraception is a realistic strategy that would save elephants without having to kill them. R. A. Fayrer-Hosken*, D. Grobler, J. J. van Altena, H. J. Bertschinger, J. F. Kirkpatrick *College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602-7385, USA e-mail: [email protected] 1. van Aarde, R. J., Whyte, I. & Pimm, S. Anim. Conserv. 2,

287–294 (1999).

2. Whyte, I., van Aarde, R. J. & Pimm, S. Anim. Conserv. 1,

77–83 (1998).

3. Kirkpatrick, J. F., Turner, J. W., Liu, I. K. M., Fayrer-Hosken,

R. A. & Rutberg, A. T. Reprod. Fertil. Dev. 9, 105–110 (1997).

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