Marine megafaunal extinctions and trophic cascades: what really happened to Steller’s sea cow?

J.A. Estes A. Burdin D.F. Doak

58

32

10

66 Felisa Smith et al. 2004 Two main questions

1. Why did the losses occur? 2. What were the ecological consequences?

• Our focus—Steller sea cow

• Our conclusion—the answer to these questions are deeply interconnected Steller sea cow

Steller’s sea cow

•A dugongid sirenian—radiated into North Pacific with onset of recent Glacial Age and polar cooling.

•An obligate kelp feeder—dentition used for feeding on marine angiosperms lost entirely.

•Patterns driven by the radiation and proliferation of the kelps.

•Suddenly disappeared in late Pleistocene

Pleistocene

1742

Commander Islands sea cows • Reportedly abundant in 1742 and during early years of the maritime fur trade • Commanders never occupied by aboriginal peoples • Evidence for early peoples and against climate change. • Extinct by 1768 The sea cow’s extinction must have been human-caused, but exactly how did this occur?

Two ideas:

1.Direct overkill

2. Indirectly via the sea otter-kelp trophic cascade Turvey and Risley (Biol. Lett. Royal Society, 2006)

• Modelled Bering Island sea cow population trajectory based on information in Stejneger’s (1887, Am. Nat.) paper

• Concluded: o Kill rates easily sufficient to explain sea cow declines and extinction o Sea otter-kelp hypothesis therefore could be discounted Table 1—Turvey and Risley

Evidence?

1768 The last sea cow Fig. 2—Turvey and Risley

Sea cow extinct 1768

Russian Discovery 1742 Two finer points

1. The magnitude of direct human mortality 2. Model based on constant K – Probably an incorrect assumption – Here’s why Table 1—Turvey and Risley

The last sea otter

1768 The last sea cow • Sea otters disappeared well before the last sea cow • Was the sea otter/kelp trophic cascade a contributing factor? Sea otters rare

Sea otters abundant 25 Kelp State (1) 20

15

10KelpDensity Urchin State (0)

5

0 0 200 400 600 800 Urchin Biomass

Questions

• Did a kelp forest phase shift follow the collapse of sea otters in the Commander Islands?

• Was the change in kelp abundance large enough and, if so, did it occur in a time window that would have mattered to sea cows? Sea Otter Abundance 100

80

60 Amchitka I. N. Adak I. Kagalaska I. 40 L. Kiska I.

20

0 Sea otter abundance(%Sea otter maximum count) Sea Urchin Biomass 400 2 - 300

200

gms 0.25m gms 100

0 Grazing Intensity 60 1 - 50 40 30 20 10 Percent loss 24hrPercent loss 0

10 Total Kelp Density

2 8

6

4

No. per 0.25 mperNo. 0.25 2

0 Estes et al., 1998 1972 1985 1987 1989 1991 1993 1995 1997 Year Adak Amchitka

Kelp Density

-2 8

4 No. 0.25m No. 0

Before decline After decline

~ 12-fold reduction in kelp density Kelp forest phase shifts

Doroff et al., J.Mammal. 2003 High Points

• Otter collapse in Aleutians occurred over a period of about 10 years (1990-2000) • Kelp forest phase shift occurred mid way through this collapse (~1995) • Otter collapse in Commander Islands followed a similar trajectory (1743-1754) • Therefore, kelp forests probably collapsed in Commanders by about 1750 Fig. 2—Turvey and Risley

Sea otters extinct 1754 Kelp forest collapse 1746-1750 Sea cow extinct 1768

Russian Discovery 1742 How might this have influenced the Bering Island sea cow population? Modelled resource limitation

• Started with same life history data as Turvey and Risely (from Anderson 2002) • created demographic model based on general sirenian life history parameters • used results from Preen and Marsh (1995) to simulate food limitation -calves from 22-2%

Cont.

• Annual starvation survival rate – 0.912 (best case) – 0.838 (worst case) – 0.737 (worst case with emigration) • Applied probabilities to natural reproduction and survival rates in the model 1500

0.912 1000

0.838 500 Population Size Population

0.737 0 1740 1750 1760 1770 1780 1790 1800 Year What about elsewhere in North Pacific? Pleistocene

1742

Commander Islands sea cows • Reportedly abundant in 1742 and during early years of the maritime fur trade • Commanders never occupied by aboriginal peoples • Evidence for early peoples and against climate change. • Extinct by 1768 40 30 20 Amchitka Island, 1972 10 0

40 30 Pisa Point, Attu Island, 1976 20 10 Modern Ecosystems 0

40 30 Casco Point, Attu Island, 1976 { 20 10 0

40 30 Stratum B 20 10 0

40 30 Stratum C 20 10 0

40 30 Stratum D 20 Frequency 10 0

40 30 Stratum E 20 10 0

40 30 Stratum H 20 10 0

40 30 20 Startum I 10 0

40 30 20 Stratum J 10 0 Simenstad et al. 1978 5 15 25 35 45 55 65 75 85 95 Test Diameter Ecological Extinctions Concluding Points

1. Direct human exploitation may well have done in the sea cows 2. But their extinction in the absence of direct exploitation was almost inevitable 3. Extinctions of other species because of the loss of keystone predators?