Wednesday, May 09, 2012

Reef Sharks and Humans?

Bikini Atoll 10 years ago after it was re-opened to the public after 40 years - these comparatively short-lived Reef Sharks had never seen people.

I've finally gotten myself the Nadon et al paper.
In essence, it comes to the conclusion that Reef Shark populations in populated areas in the Pacific have plummeted by 90%, as reported e.g. here, here, here and here. Apparently, Julia Baum asserts that the decline is principally due to fishing and incidental bycatch.

Probably true - and yet, I am not totally convinced.
Now mind you, I am not a sufficiently trained researcher and may have missed some of the finer points in the paper - but then again, I was intrigued by this really interesting post by Para_Sight who points out that the causal connection may not be quite so direct, and I cite.

A binary relationship between the abundance of sharks and that of people is effectively saying that they are mutually exclusive: people = no sharks, no people = sharks.
That’s a pretty disappointing thought. Of course it doesn’t tell us the mechanism, or even if the relationship is causal in any way, but I don’t think it’s a huge leap to suggest that human impacts on reef diversity and function in general, especially overfishing, are likely to put a pretty negative pressure on reef shark populations. If this proves true then it may not be that humans are doing anything to the sharks per se, just not looking after the reef generally, and that is being reflected at the top trophic level.
However you slice it, their results are more grist to the mill that we need to be doing a better job with the conservation of
both reefs and sharks, because sometimes those two things are inextricably intertwined.

I could not agree more!
If we want to preserve a species we must preserve its habitat, #5, and this not only including the reefs but all of the hot spots like seasonal aggregation sites and above all, the nurseries!
But that's not where I want to go with this.
Let me elaborate.

1. Propensity to approach Divers and Boats.

Intuitively, I feel that the 90% number may be too high
, and this due to the chosen survey method, i.e. "towed-dive surveys" where paired SCUBA divers record shark sightings while being towed behind a small boat.
From the paper.

During each survey, a diver being towed behind a small boat recorded the identity and size of all fishes larger than 50 cm total length (nose to longest caudal fin lobe) encountered in a 10-mwide belt (Richards et al. 2011). To ensure surveys represented a near-instantaneous snapshot, divers counted only individual fish in a 10 × 10 m area in front of them and were careful not to record the same fish more than once.
All observers were experienced scientific divers with extensive training in fish identification. Divers were towed for 50 minutes on each survey at approximately 45 m/min, which is much faster than the swimming speed of divers conducting belt transects (typically 8 m/min).
We used a global-positioning-system unit on the tow boat to calculate transect lengths. Average tow length was 2.2 km. Surveys followed fixed isobaths (generally 15–20 m depths) and were positioned evenly around an island, with the aim of covering most of the circumference of each island at the targeted isobaths (tows around small islands were closer to each other than those around large islands).
We analyzed only the towed-diver surveys that were conducted on forereefs (seaward slope of a reef) between 2004 and 2010 (n = 1607).

Very compelling - and yet...
Check this out.

This is Bikini Atoll in 2003.
I hear that the Sharks have alas been fished away, but here is a report from 2000, and I cite.

After a few hours of casting along the reef, we approached a quarter-mile wide channel separating two idyllic tropical islands festooned with palm trees. The crew was smiling as Maddison said, "Watch this."

Within minutes an armada of shadows appeared, heading our way.
The dark shapes turned out to be hundreds of gray reef sharks, which began swimming around the boat, their aggressive mood indicated by arched body postures. The scary part was that we hadn't put any chum in the water!

Totally déjà vu!
Having been around for a while and done quite a bit of exploration several decades ago, I distinctly remember witnessing this behavior whenever we did visit remote and pristine locations. We would get to the reef with the dinghy and within minutes, the Sharks (often Grey Reefs that are 71% of the Sharks counted in the surveys discussed in the paper) would be rushing to the craft.
Moreover, once in the water, the Sharks would actively approach the divers, sometimes in a quite assertive way. However as time went by and those dive sites would become more popular and thus more crowded, I remember witnessing a gradual retreating of the Sharks.
As an example, when I first dived Cocos in the early 80ies, Chatham Bay was full of Hammerheads all the way to the surf line, and the seaward side of Cascara and Pajara would always yield a lot of Hammers, Silvertips and Marbled Rays that would easily approach the divers. Now, those high traffic areas feature very few Sharks that appear to have retreated to the more remote locations like Dirty Rock, Shark Fin and Alcyone where they are also generally much more skittish.

And what about the small boats?
Reason would have it that in their majority, small boats around populated islands would be engaged in fishing.
In fact, the paper states

We assumed human population was a reasonable measure of human effects in this region because most of the surveyed populated islands (including all population centers) have been settled for centuries, have broadly comparable levels of fisheries development (including widespread use of motorized boats and modern fishing gear) and reef fisheries with a mix of recreational, subsistence, and commercial fishing activities.

Reason would also have it that those Sharks who would have most readily approached those boats would have been the first to get killed either as proper catch or in retribution for being a nuisance like what has apparently happened in the GBR - whereas more timid Sharks would have had a higher chance of surviving and thus passing on their propensity to avoid boats to the next generation.
Could it be that over the many years, this would have led to more boat-wary Sharks in populated areas due to the selective extirpation of the bolder gene pool?

Long story short?
  • Maybe when sampling remote islands, the small boat towing the observers did attract Sharks (in the case of the Grey Reefs, possibly even out from the passes where they usually reside and to the forereefs that were being monitored), thus leading to a positive bias when establishing the baseline count.

  • Maybe when sampling inhabited islands, the boat noise did repel Sharks and thus lead to a negative bias.
The consequence of the above would lead to a double observation bias and result in an exaggerated rate of decline and confirm my purely intuitive caveat.

Yes at this stage, this is highly speculative.
But is this plausible and if so, would it be worth testing, and how?

2. Human Effect - only negative?

Reefs surveyed by towed divers 2004–2010 in the Pacific Ocean (triangles, survey reefs; white stars, large human population centers; PRIA, Pacific Remote Island Areas).

This is the area that has been surveyed.
I'm sure that the observations are generally accurate, albeit maybe biased as per the above - and yet, they may not be the whole story.

Take French Polynesia.
It features highly populated islands where Shark populations are however healthy. My interpretation is that there is a vibrant Shark tourism industry that has provided for an economic incentive for not fishing for Sharks, this even before the current Shark protection measures. Also, due to the tests in Mururoa and Fangataufa, the archipelago has been heavily patrolled which has likely kept potential poachers at bay,

And here's another personal observation.
In 2002, I organized a 13-month exploratory diving expedition throughout Micronesia and Melanesia aboard a large roving liveaboard vessel.
Here is the itinerary, click for detail.

In essence, we started in Bali and then did Kupang, Irian Jaya, Palau, Yap, Chuuk then down to New Ireland, over to Manus and Wewak, back to New Britain, then Bougainville all the way past Ghizo to Honiara, then back to Milne Bay.
Always in search of the most pristine environments and of Sharks, we did target the most remote and least populated locations between the principal islands where we would stop to re-supply. Especially in the Micronesian atolls, we specifically dove the likely hotspots, i.e. the reef passes where we would attract scores of Grey Reef and Silvertip Sharks with the infamous bottle. When close to the principal islands, we would co-operate with chosen local dive operators and visit their flagship dive sites, like e.g. Blue Corner in Palau.

Our findings were completely counter-intuitive.
To my great dismay, the most remote and least populated reefs had been completely fished out. Several of the Micronesian atolls featured wrecks of long liners and those reefs were covered in fishing gear, mainly long lines and ghost nets. Conversely, moderately populated islands had no Sharks right in front of the villages but plenty just a short distance away, and many of the principal islands did feature surprisingly healthy stocks.

My interpretation is that there is no such thing as "remote and pristine" anymore.
The fishing fleets have the resources, the technology and the willingness to go looking for Fish anywhere, and will wreak utter havoc when and where nobody is watching.
Conversely, especially Melanesia has a strong tradition of reef tenure where the traditional owners will vigorously, and often violently defend their fishing grounds against any intrusion.
Finally, like in French Polynesia, many of the principal island have well established Shark viewing tourism operations.

For me, this was a seminal observation.
Ever since that voyage I'm of the conviction that the only way to conserve biodiversity is to abandon the utopian vision of there being anything "natural" left. Instead, we must recognize that our influence extends to everywhere and that instead of bemoaning a past that will never come back, we must concentrate on managing what is left. Check out the current definition of wilderness & you will discover that this has now very much become a relative concept and a managed space.

But I'm digressing as usual.
The paper says this about protection.

We did not include protection level in our analyses because the region’s large marine protected areas were established only recently (e.g., 2006 in the northwestern Hawaiian Islands) and because protected areas cover only small percentages of the total coastline in populated areas (e.g., 5% around the main Hawaiian Islands). There is also some evidence that only areas that are strictly off limits to humans effectively protect reef sharks (Robbins et al. 2006). Moreover, in the larger, more isolated protected areas (e.g., northwestern Hawaiian Islands), remoteness rather than formal protection is probably the main factor limiting fishing because enforcement is generally light.

Maybe the above is just too narrow.
From my personal observations, there are other mechanisms that may well confer a substantive degree of protection and where the presence of humans is more of a positive than not.
But those are just nuances - the general gist of the paper is certainly correct.

Anyway, just a bit of food for thought.
Bon appétit!

PS more evidence for Reef Shark population declines here!


OfficetoOcean said...

Brilliant blog. That's all I can add really...

Anonymous said...

I think you raised some great points. Taking the examples from Hawaii specifically, here are further flaws in the paper.
1) there is no shark fishery in Hawaii. granted there are people who shoot sharks, but to claim this activity has removed 90% of the population seems a big exageration
2) the main flaw, as you mentiioned, is the technique. Diver surveys are inherently biased in that they will attract sharks in remote areas, and probably repel them in locations where humans are present. Take a look at fishing based surveys of the main hawaiian islands. Catch rates are always high with species that were never seen on dive surveys. Even in remote areas, fishing rates of tiger sharks are high, whereas the diver surveys never saw this species.
Finally the study also didnt really take into account differences in depth, simply put the inhabited islands (at least in Hawaii) reach deeper water much more rapidly. When you take into account that no survey was done > 30 m, this adds further bias.
Overall, I am sure that shark populations are smaller around islands with humans. but the 90% is certainly an exageration.

DaShark said...

Thanks for that - very interesting!

I'm happy to hear that Sharks are not anymore being targeted in Hawaii.

Just a few years ago, I witnessed with my own eyes how the game fishermen that were trolling for Billfishes around the FADs off the Big Island were throwing in baited buoys to dispatch the Oceanic Whitetips they considered a nuisance.
In fact, the only OWT we found following the Shortfin Pilot Whales was completely spooked and dashed away as soon as we hit the water - and this despite of a couple of juicy & undoubtedly illegal offerings.

Anonymous said...

Very interesting post and you point out some important issues with the paper.
Regarding survey technique for sharks, that's always a big issue and frequently generates a lot of discussion about the results of abundance estimate studies. There is a recently published paper that analyses the performance of different survey techniques in estimating shark abundance, ( Although they don't analyse manta tow survey -which is a pity- the paper does give a good idea of how biased different techniques can be.

Also, it's worth to consider (as you point out) the differences in the levels of interaction, and thus differences in levels of pressure, between humans and sharks across the Indo-Pacific.
Well done!

DaShark said...

Thanks for that, appreciate!

Boy that sure is a hugely technical paper!
Just goes to show how difficult it is to establish the "facts" in an environment that is so inaccessible and so riddled with variables.

Anonymous said...

Thanks Mike-and you are right OWT are often targeted by fishermen due to their interfering with pelagic fishing. In fact they may well be one of the most heavily hit species in the Hawaiian Islands.
Also, I dont dispute that there is some killing of sharks in Hawaii, as well habitat degradation and reduced levels of prey. All of these are going to lead to lower shark abundance in the main Hawaiian Islands. However, there is no targeted fishery for sharks and that is partially due to social reasons, as sharks are considered 'amakua' by many Hawaiians, hence killing them is very taboo. My main point is that fishing rates of sharks in the Hawaiian Islands does not match the 90% decline in the population suggested from the tow surveys.

Marc Nadon said...

Great post!

I followed the link from the “Deep Sea News” blog. You all raise valid questions and I’m afraid I don’t have definite answers. However, here are a few comments I would like to add to the discussion:

1) About diver attraction or repulsion

We don’t really have extra data to address this, so I can only talk about my impressions. First, the discussion focuses on the hypothesis that reef sharks are afraid or less curious of boats/divers around inhabited areas. But couldn’t the reverse also be true? If reef sharks aren’t targeted in Hawaii and food (i.e. reef fish) is scarce, wouldn’t reef sharks be attracted to boats or divers in search of easy pickings from injured/disabled fish? I simply haven’t seen enough reef sharks in the main Hawaiian Islands (MHI) and other inhabited areas to have a clear idea (despite hundreds of dives).

We very rarely see the kind of extreme attraction behavior described at Bikini Atoll. I can only think of one event where the oceanography team was deploying some instruments from the surface and had about 100 gray reefs circling their line… Most towed surveys in pristine areas will encounter one or two sharks over a 2 km swath (i.e. not a hundred sharks on one survey and zeroes for the rest). This being said, there is generally some level of attraction behavior in gray reef sharks.

Another point: I haven’t really noticed high level of curiosity in whitetip reef sharks, even at pristine reefs (I think diver-effects are much reduced in this species). Yet their numbers are also down around 80% (Hawaii) and 90% (Mariana) compared to pristine areas with similar oceanographic conditions.

Finally, we are currently deploying baited and un-baited cameras for fisheries- independent surveys. It will take months before this data is properly analyzed. All I can say is that we haven’t really seen many reef sharks on these camera drops around populated areas (at depths going to >100m). Hopefully this will help reach some conclusion on the issue of diver bias.

2) Fishing based surveys around Hawaii (Papastamatiou et al. 2006)

Anonymous points out that fishing-based surveys (looking at catch-per-unit-effort) show “catch rates are always high with species that were never seen on dive surveys”. I’m guessing this is based on the Papastamatiou paper (please correct me if I’m wrong).

The main shark caught around the MHI is the sandbar, yet we’ve never observed one on any survey, anywhere (2000+ and counting). The paper points out that this species is mostly caught with hooks set between 50-100m, which is much deeper than our surveys (gray reefs were caught mostly at shallower depths). This is a deeper species. We would still expect shallower reefs to be inhabited by reef sharks, as they are in all pristine areas we visit.

This paper doesn’t really stipulate what a “high” catch rate is. Catching a few tiger sharks every 100 hooks doesn’t really inform us on their density and if we should have seen more on towed surveys then we have. The article does point out that CPUE for all species except the sandbar are much lower in the MHI than the remote NWHI.

3) Is a 90% decline exaggerated?

The 90% number is actually the lower range of our estimate (97% being the upper limit of our 95% confidence interval). I’m not sure I find this number so surprising. I’ll simply point out that since reef sharks have a “slow” life history, it doesn’t take a high fishing mortality rate to get their populations trending downward. A slow decreasing trend decade-after-decade will invariably lead to very low population numbers. I’ll also point out that reef fish biomass is down by about 75% around populated areas (Williams et al. 2011) and they represent about ~70% of reef shark diet.

Our paper is certainly not the last word on the status of reef sharks, but we do believe our conclusions are fairly robust.

Sorry for the long post! As DaShark pointed out, this issue gets complicated quickly. Thank you for the thoughtful comments.

DaShark said...


Thank you so much for taking the time to write a comment here Mark!
Very interesting - and very depressing as well!

Funny you should mention the Reef Whitetips.
When using the infamous bottle, we discovered that contrary to the Greys and Silvertips that would be immediately home in, they would instead flee precipitously!
I've also found them to behave very differently in different places. Being a crepuscular Shark, I would normally see them resting during the day, but whereas they would do so in the open in places like, say, Cocos and Bougainville Reef in Australia, in other places they would be very cryptic and hide in crevices - and maybe be less noticeable to a roving observer.
And being, at least in my view, the sharky counterpart to the moray eel and thus occupying a very similar trophic niche, they are ubiquitous in Cocos where morays are rather rare, and completely absent in neighboring Malpelo where there are thousands of morays - this despite of nearly identical habitats and quite obviously not due to human interference.
Yes it sure is complicated! :)

But I'm obviously digressing.
I'm really, really looking forward to a comparison to your video data, especially those from the BRUVs!

I'm also really intrigued by your remark that a decline in reef fish will entail a decline in Sharks - totally logical and yet, most of the arguments of the Shark conservationists appear to focus on targeted fishing and bycatch, and on top-down effects as in trophic cascades.
As I said, I'm merely an interested Shark conservationist and not a researcher: are there any papers that have tried to describe that causal bottom-up connection - or hasn't anybody really bothered because it is ultimately so trivial?

Anyway, really appreciate your clarifications, thank you!

Marc Nadon said...

No problem! This is an interesting discussion and I don't mind taking some time to answer the valid points you and others have raised.

I think many scientists and conservationists focus on reducing top-down effects (i.e. by-catch or targeted killing) simply because it's the more obvious negative effect and the easiest to tackle.

Re-building reef fish stocks to increase reef shark abundance might be a harder sell.

I am not aware of papers addressing the issue of bottom-up control on reef sharks specifically. It is an obvious issue though. If 75% of a predator's prey population is removed and there is no clear alternative diet, it is simply impossible for that predator population to remain at the same level.

Thanks for this interesting discussion and good work on your blog!