Fish behavior -- in particular, algal grazing and, to a lesser extent, aggression -- varied over both chronic and acute differences in human presence. Quantile regression revealed an apparent upper bound of individual herbivorous fishes' bite rates across all sites, resulting in a wedge-shaped distribution whereby maximum bite rate decreased as the number of humans present during the observation period increased (Fig. 5A; tau = 0.99; R2 = 0.02, t = -2.18, p = 0.03). When only parrotfishes were considered, site was revealed to be a significant factor in parrotfish bites per unit time (F(3, 38) = 5.156, p = 0.004), prompting further analysis using only the most heavily-visited sector in the bay (Keyhole; see Fig. 1C map). This analysis revealed that aggregate parrotfish bites per unit time decreased dramatically at this site from full closure (4.4 bites/minute) to post-COVID re-opening (0.6 bites/minute; Fig. 5B; t(4.4858) = 3.6857, p = 0.01724). Lastly, our zero-inflated regression model via maximum likelihood revealed an apparent upper bound in the time that fishes spent attacking one another (Fig. 5C). Specifically, at lower levels of human presence, fish exhibited a wide range of time devoted to aggression, while at high human presence, little time was devoted to aggressive behaviors, resulting in a detectable negative effect of human density on the time spent by fish attacking each other (Table S4). Other behaviors quantified as time budgets, including feeding, cleaning, and burrowing, did not exhibit differences due to either chronic or acute human presence (Table S5).
By curtailing human activities, the COVID-19 pathogen indirectly affected coral reef ecosystems via changes in water clarity and the numbers and behavior of reef animals. Specifically, when human visitation to the Hanauma Bay Nature Preserve ceased due to the COVID-19 anthropause, water clarity improved, and increases were detected in the presence of endangered Hawaiian monk seals, the abundance of fish, and the rates of parrotfish herbivory (i.e., algal removal) at heavily visited sites in the bay. Following the anthropause, when humans had returned to the bay, fish were (counterintuitively) attracted to the immediate presence of snorkelers, such that fish abundance increased over scales of seconds to minutes when humans were present within a given area of reef. Overall, these results suggest that chronic human presence likely has a measurable, inhibitory effect on multiple ecosystem parameters, including the key ecosystem function of herbivory that is critical to maintaining coral reef health.
The striking difference in water clarity between the COVID and post-COVID periods of the study demonstrates significant impacts from visitors to the bay, most likely due to sediment resuspension, which is magnified as human density increases. Water clarity was not assessed prior to the COVID-19 closure of the bay when up to 3000 visitors were utilizing the bay, but this pattern suggests that it may have been lower still under pre-COVID conditions with fourfold-plus-higher visitation intensity. This finding is in agreement with results from the COVID-19 anthropause in India, where coastal turbidity decreased during COVID-19 lockdowns. Water quality is known to be an important determinant of overall coral reef health, affecting multiple key taxa through different mechanisms. For example, over a regional scale on Australia's Great Barrier Reef, water quality was found to be strongly predictive of both coral species richness and macroalgal cover, with the former inversely related and the latter positively correlated, and high levels of suspended sediment reduced coral recruitment on Molokaʻi, Hawaiʻi. Numerous other studies have found similar results at smaller scales, including examples of snorkeler- and diver-derived sedimentation effects on coral disease prevalence, live coral cover, coral recruitment, macroalgal cover, and diversity of corals and fishes. Because sedimentation impacts on coral reefs are magnified with increased intensity, duration, and frequency of resuspension disturbances, reducing the number of snorkelers and waders, the amount of time spent in and around the reef, and/or the number of visitor days would likely reduce the impact of snorkeler-derived effects on coral health via reduced water quality.
We found Hawaiian monk seals were roughly half as likely to visit the Hanauma Bay Nature Preserve when humans were present in the pre- and post-COVID periods versus the COVID period, during which humans were absent. This result is in accordance with previous studies of related pinniped species (e.g., the Mediterranean monk seal (Monachus monachus)) and other pinniped species worldwide. Our results suggest that even the dramatically reduced visitor capacity in the post-COVID period caused apparent effects on monk seal haul-out behavior. It therefore remains unknown what level of human visitor density should be maintained in order to minimize or eliminate these effects. Allowing for longer periods of 'rest' for the bay in which no humans are present could potentially increase the number of days monk seals could utilize this habitat. However, whether seals are likely to respond to such a change is unclear, given that with one or more days closed to visitors per week, seals would still encounter humans on the remaining days when exploring the bay as a potential haul-out site.
Our finding that overall reef fish density was lowest under the highest levels of human visitation to Hanauma Bay (i.e., the pre-COVID period) qualitatively matches patterns seen elsewhere such as Akumal, Mexico. As with that study, the mechanisms for this pattern in the present study remain untested, but are likely due to inherent threat-avoidance behaviors of fishes to humans. We conversely found that in the post-COVID period, when visitors had returned to the bay, fish were strongly attracted to the presence of snorkelers over scales of seconds to minutes, a likely sign of increased food availability surrounding snorkelers due to re-suspended organic matter from snorkelers' fins disturbing sediment. This result is in line with Brock et al.'s finding roughly 20 years ago that significantly more fish were observed in Hanauma Bay on days open to the public vs. closed days, a likely result of food provisioning by humans, which had been done for decades at the time of that study and ceased just prior to the study's start. A precondition for a lack of fishing pressure and habituation to snorkelers is essential to this scenario. Our contrasting findings (i.e., Fig. 4A vs. 4B) result from different time scales of human presence, suggesting different fish behavioral responses across temporal scales and specifically that long-term risk avoidance is offset in the short term by the reward of food availability. Although untested, short-term density changes due to both chronic and acute human presence are presumed to be due to changes in fish behavior rather than population growth, suggesting that fish behavior may play a key role with regard to mediating human impact.
Furthermore, herbivore grazing behavior was dramatically reduced in the post-COVID period relative to the COVID period when humans were absent, and individual herbivore bite rates were also reduced as a function of increasing visitor numbers across these two periods. This effect is not likely due solely to differences in the density of herbivores across the different study periods because there was no significant difference in overall fish density between the COVID and post-COVID periods. Additionally, the post-COVID period had lower grazing rates than the COVID period. These findings collectively suggest that snorkeler presence can suppress the key ecosystem function of herbivore grazing.
By halting all human visitation to the study's heavily visited coral reef ecosystem, the COVID-19 pathogen indirectly instigated a clear-cut 'natural experiment' that would not have been possible in its absence, and in the process revealed a number of important considerations and potential prescriptions for management strategies of the Hanauma Bay Nature Preserve and other coral reef ecosystems worldwide. First, reduced human visitation allowed multiple biophysical ecosystem parameters to shift towards levels present when unimpacted by direct human presence. Secondly, by inhibiting the grazing of benthic algae by herbivorous parrotfishes, one of the key groups responsible for maintaining balance between coral- and algal-dominance of reef benthos, human visitation to this iconic coral reef (and perhaps other reefs globally) may inadvertently promote ecosystem decline. Our results add to the growing body of knowledge resulting from the COVID-19 anthropause and other situations that reducing human visitors to a diversity of other natural areas (both wilderness and other) often leads to rebounds in abundances and changes in behavior of wildlife and subsequent restoration of key ecosystem structure, processes, and function, though studies of these indirect effects remain scarce.
To our knowledge, previous studies resulting from the COVID-19 anthropause have not shown diverse, biophysical effects from a single location as we show here. Importantly, at least two of the effects observed in this study -- reduced herbivory and increased turbidity -- may act synergistically to threaten coral growth and survival beyond either factor in isolation. Nonetheless, our results suggest that this particular location has begun to somewhat mitigate these negative effects by re-opening, post-anthropause, with reduced human visitor density (i.e., a maximum of 3000 visitors/day pre-COVID to a maximum of 750/day during the study's post-COVID period). This reduction may help explain why there was no detectable difference in overall fish density between the COVID closure and post-COVID periods. It may also help explain the lack of difference among fish behavior allocation, other than parrotfish herbivory, that were measured only in these latter two periods (due to lack of pre-COVID data).
Implementing visitor limits for currently unrestricted reefs elsewhere in Hawai'i and the global tropics, or further reducing visitor limits where they currently exist, has the potential to regain lost ecological function and reduce negative human impacts on reefs. While coral reef tourism generates an estimated US$36 billion globally each year and nearly US$1 billion in Hawai'i alone (Hawai'i DLNR 2023), it is important to consider the need for balance between ecological restoration goals and the economic benefits of reef tourism. These goals may not be necessarily at odds, given that past research has shown visitors are often willing to pay a higher price to visit reefs that are perceived or marketed as 'pristine' rather than degraded, thus potentially offsetting lost revenue due to visitor caps.
Despite these findings, many questions remain about the impact of human visitors on both the Hanauma Bay Nature Reserve and other reef systems. First, this study is one of the few to date that documents if and how human-induced animal behavior change on individuals, populations, and communities results in cascading effects on ecosystem functions in any ecological system, yet understanding these effects is important for wise visitor and resource management decision-making. Secondly, our study design did not allow us to answer the question of what the lower threshold is for the onset of negative effects (i.e., what density of visitors could exist without negatively affecting ecosystem structure or function), although our research does suggest that a roughly linear decline in maximum herbivory occurs as human density increases. Similarly, we did not observe negative impacts on other behaviors quantified as time budgets (e.g., feeding, cleaning, and burrowing); therefore, it remains unknown what density of human visitors would likely trigger suppression of these and other unmeasured behaviors and ecosystem metrics. Additionally, Hanauma Bay is one of the few reef systems in the main Hawaiian Islands that is fully protected from fishing and other extractive uses, and therefore maintains far higher abundance and biomass of reef fishes than most other reefs in the MHI archipelago. How these results translate to other, more impacted reefs in the main Hawaiian Islands and other regions globally remains unknown. Importantly, one interesting insight arising from these findings is that the COVID-19 anthropause affected both the abundance and behavior of reef fishes and monk seals, which suggests that to fully quantify the effect on wildlife populations, future studies should aim to measure multiple parameters among diverse marine populations.
Collectively, these results paint a picture of the various and unexpected ways in which a novel human pathogen indirectly affected a coral reef ecosystem by altering human behavior patterns. In so doing, this study highlights the interconnectedness of human and ecological systems, pointing to the need to consider potential downstream implications of seemingly unrelated human societal decisions and policies on wildlife and ecosystem management. Given the vital importance of reef tourism to local economies and the cultural, spiritual, and economic value of reefs to Indigenous and other local communities, managers must find a balance between visitor management and ecological preservation of coral reefs within Hawai'i and elsewhere in the global tropics.