Does whale watching in Southern New England impact humpback whale (Megaptera novaeangliae) calf production or calf survival?

Biological Conservation 142 (2009) 2931–2940

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Does whale watching in Southern New England impact humpback whale (Megaptera novaeangliae) calf production or calf survival? Mason Weinrich *, Claudio Corbelli The Whale Center of New England, P.O. Box 159, Gloucester, MA 01930, USA

a r t i c l e

i n f o

Article history: Received 1 February 2008 Received in revised form 7 July 2009 Accepted 23 July 2009 Available online 29 September 2009 Keywords: Humpback whale Whale watching Reproduction Birth rate Survivorship Tourism effects

a b s t r a c t There is growing concern about the effects of wildlife tourism on biologically important parameters in target species and/or populations. We tested whether whale watch vessel exposure affected either the calving rates or calf survival to age 2 in humpback whales (Megaptera novaeangliae) on their feeding grounds off of southern New England, where individually identified whales have been studied intensively for decades and whale watch pressure is intense. Whale watch exposure did not correlate with either the calving rate (# of calves/# of years sighted) or calf production and survival of individual females, although a breakpoint analysis showed a slight negative trend up to 1649 min (or 20 boat interactions). In some comparisons, whales with more exposure were significantly more likely to produce calves and to have those calves survive. Logistic regressions including exposure and prey variables also failed to show negative effects of exposure in predicting calf productivity or survival. A limited comparison of calves seen only in an alternate habitat without whale watching showed similar return rates to those in the exposed area. Our data include limited suggestions that some animals (i.e., females alive when whale watching started) might be more susceptible to impacts than others. However, we found no direct evidence for negative effects of whale watch exposure, and suggest that short-term disturbance may not necessarily be indicative of more meaningful detrimental effects on either individuals or populations. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction In recent decades, there has been a rapid growth and interest in wildlife tourism world-wide, whether it is to view African wildlife on safari, to experience a tropical rain forest, or to see whales and dolphins in the open ocean (Tapper, 2006). This growth has been accompanied by concerns about the ultimate effect that increased viewing and its resultant interference may have on targeted individuals and/or populations (Newsome et al., 2005; Tapper, 2006). One area of growing concern has been for the impacts of tourist viewing, or ‘‘whale watching,” on cetaceans. Studies have suggested that cetaceans sought for prolonged, close-up encounters, and/or approached by numerous vessels with erratic paths may react by changing behavior, avoiding vessels, or displaying annoyance (Corkeron, 1995; Williams et al., 2002; Lusseau, 2004; Scheidat et al., 2004). If such disruption is repeated above a certain threshold, it could lead to impairments in an individual’s breeding, social, feeding and resting behavior. If enough individuals are so affected, this could contribute to secondary deleterious effects on a population’s long-term reproductive success, distribution or access

* Corresponding author. Tel.: +1 978 281 6351; fax: +1 978 281 566. E-mail address: [email protected] (M. Weinrich). 0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2009.07.018

to preferred habitat (Fair and Becker, 2000; Bejder and Samuels, 2003; Higham and Lusseau, 2004). This relationship is elucidated in the Population Consequences of Acoustic Disturbance (PCAD) model, which has now been accepted as a theoretical framework of understanding population-level consequences of whale watch exposure (IWC, 2007). However, limited long-term data sets mean that there are few opportunities to apply the PCAD model and determine whether such population-level effects exist. Those studies that have been conducted have usually recorded changes in animal range, habitat use or distribution (Duffus, 1996; Samuels and Bejder, 2004; Lusseau, 2004, 2005). Recent critiques, however, suggest that even measures of displacement can only be determined for a sub-set of the population that is not obligated to remain in a habitat where there may be critical resources (Beale and Monaghan, 2004; Creel et al., 2002; Dyck and Baydack, 2004). More recently, impacts have been studied by correlating female bottlenose dolphins (Tusiops aduncus) reproductive rates with the amount of vessel exposure in Shark Bay, Australia (Bejder, 2005; Bejder et al., 2006), where females exposed to higher vessel activity over 11 years had lower reproductive rates than those with less exposure. Based on a consideration of the existing information, in 2006 the whale watching sub-committee of the Scientific Committee of the International Whaling Commission concluded that ‘‘there is new compelling evidence that the fitness of individual odontoce-

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tes repeatedly exposed to cetacean watching vessel traffic can be compromised and that this can lead to population effects. The sub-committee recommends that similar studies looking at individual fitness of cetaceans be carried out wherever possible. However, in the absence of these data it should be assumed that such effects are possible until indicated otherwise (italics added by author). The sub-committee strongly encouraged the development of similar studies on large whales” (IWC, 2007). Whale watching tours began in New England in 1975, and within a decade the regional whale watching industry became the largest in the United States and one of the largest in the world (Hoyt, 2001). In New England operators established their own brand of commercial whale watching with strong educational and scientific components. Tour boats have been used here as research platforms since the mid-1970s and have resulted in many papers about local whale populations, including fin whales (Balaenoptera physalus; e.g. Seipt et al., 1989), humpback whales (Megaptera novaeangliae; e.g. Weinrich, 1991; Weinrich and Kuhlberg, 1991; Clapham et al., 1993; Weinrich et al., 1997), minke whales (Balaenoptera acutorostrata; Murphy, 1995) and Atlantic white-sided dolphins (Lagenorhynchus acutus; e.g. Weinrich et al., 2001). Whale watching in New England primarily targets humpback whales (Beach and Weinrich, 1989; Hoyt, 2001), which use the Gulf of Maine as a feeding ground from April through December, and spend the winter months breeding in Caribbean waters (Martin et al., 1984; Katona and Beard, 1990; Smith et al., 1999; Stevick et al., 2003a). These whales represent a sub-population of 902 animals (595–1209, 95% CI; Clapham et al., 2003) of the larger North Atlantic population, which is comprised of 11,570 individuals (10,290–13,390, 95% CI; Stevick et al., 2003b). Humpback whales in the study area prey on a number of small, abundant swarming prey, including herring (Clupea harengus), and, to a lesser extent, euphasiids (especially Meganyctiphanes norvegica; Stevick et al., 2008), but sand lance (Ammodytes spp.) are the dominant and preferred prey (Payne et al., 1986, 1990; Weinrich et al., 1997). The Gulf of Maine humpback whale population has been the subject of on-going longitudinal study since the late 1970s (Clapham, 2000), providing a unique opportunity to examine potential effects of whale watching on reproductive fitness of female humpback whales. Whale watch boats in the Gulf of Maine operate under a voluntary code of conduct, or guidelines, that are officially endorsed by the National Marine Fisheries Service, the federal agency in charge of managing whale populations in U.S. waters (Beach and Weinrich, 1989).1 The guidelines were introduced originally in the mid-1980s, and revised in the late 1990s to include a series of concentric speed restrictions around whales to address growing concerns over the risk of whale collisions. The guidelines have maintained a suggested minimum approach distance for one boat to 33 m (100 feet) of the whale, with an additional two ‘‘standby” vessels allowed within 100 m (300 feet). These guidelines are less restrictive than the majority of other guidelines or regulations world-wide (Carlson, 2007), which often contain a 100 m minimum approach distance. Although compliance of boats to most of the Gulf of Maine guidelines has not been measured, Wiley et al. (2007) showed that there was poor compliance for vessel speed guidelines, and this is likely the case for minimum approach distances as well. When the size of the whale watch industry is combined with the minimally restrictive approach guidelines and the lack of compliance where measured, the subjected population may be at risk of effects from whale watching activities.

1 Full details on New England whale watch guidelines are viewable at http:// www.whalecenter.org/conservation/wwrules.htm.

2. Materials and methods 2.1. Study locations Humpback whales were observed from whale watching vessels on their feeding grounds in the southern Gulf of Maine, primarily around Stellwagen Bank and Jeffreys Ledge (Fig. 1) between April and November from 1980 to 2006 (Table 1). Both of these areas are submerged glacial deposits that, combined with local currents, create substantial upwelling and nutrient productivity. Because of the length of the study, the number of whale watching companies and vessels varied throughout; however, each year we placed observers on board the vessels of 2–4 operators, some of which had multiple boats, out of Gloucester, MA (1980–2006), Boston, MA (1992–2006), Salem, MA (1994–2003), and Provincetown, MA (2002–2005). Each company ran 1–3 trips per day per vessel. Boats used were typically powered by 2–4 diesel engines, propeller driven (although two jet drive catamarans were used out of Boston (starting in 1998) and Provincetown (2002–2005)). Each whale watch was typically 3-1/2–5 h long, and included approximately 60–90 min of whale viewing. Boat size, speed, and capacity increased steadily from 1980 to 2000, and remained relatively consistent from 2000 onward. For most of the study, vessels were 20–30 m (with some as long as 35 m). Boats typically cruised at either 13–20 kts (single hulled vessels) or 25–35 kts (catamarans introduced in 1998). Data from whale watch vessels were supplemented by dedicated cruises to the Great South Channel, a more distant, offshore habitat used by the same population (Payne et al., 1990; Kenney and Wishner, 1995; Robbins, 2007) that received little, if any, whale watch traffic (Table 1). Such cruises usually lasted a full day, but several multi-day voyages (up to 5 days long) were undertaken as well. The data collected on these cruises allow an out-

Fig. 1. The study area.

M. Weinrich, C. Corbelli / Biological Conservation 142 (2009) 2931–2940 Table 1 Effort data for the study, as well as the data used to calculate mean number of humpback whale sightings per cruise. Year

# Days

# WW trips

# Humpback sightings

Sightings/ trip

# GSC days

1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005

53 96 121 143 159 165 142 142 153 153 161 168 164 150 132 150 150 176 169 191 183 193 191 193 187 175

58 202 529 624 733 762 433 413 605 560 515 503 521 437 280 538 468 781 718 873 842 835 892 833 751 711

515 1729 5743 5404 7192 6188 1252 809 8618 7425 8201 5271 7845 1899 962 1007 4949 9762 12,167 13,891 6020 5487 2959 4426 1428 2985

8.88 8.56 10.86 8.66 9.81 8.12 2.89 1.96 14.24 13.25 15.92 10.48 15.06 4.35 3.44 1.87 10.57 12.50 16.95 15.91 7.15 6.57 3.32 5.31 1.90 4.20

0 0 0 0 0 0 2 8 1 0 0 0 0 0 0 4 2 3 0 2 1 4 3 2 10 4

group, albeit of limited size, of females and calves who were not exposed to whale watch traffic in some years (although it should be noted that the vessels from which the observations were made were not fundamentally different from whale watch vessels). 2.2. Whale watch measures Data on the individual identification and behavior of humpback whales were collected aboard whale watch vessels by Whale Center of New England staff. Methods for data collection are detailed in Weinrich (1991), Weinrich and Kuhlberg (1991), and Weinrich et al. (1997). Briefly, whales’ dorsal fins and fluke pigmentation patterns were photographed for individual identification (Katona and Whitehead, 1981; Blackmer et al., 2000), and individuals were identified using a catalogue of Gulf of Maine humpback whales housed in Gloucester, Massachusetts. Data included the start and end time of each animal’s observation, and the identity of any other whale watch vessels within 1 km and/or those sharing the same focal animals. A mother–calf pair was defined as an adult whale (the mother) seen in close association (within a body length and coordinated in her behavior) with a whale (the calf) approximately half her size (visually estimated), for over 30 min in a single sighting or (typically) in multiple within-year sightings (Clapham and Mayo, 1987, 1990; Sardi et al., 2005). Calves expose their tail flukes when diving less often than adults (Blackmer et al., 2000), making it sometimes more difficult to obtain high quality images of their fluke patterns. In cases when expert photo matchers at the Whale Center of New England deemed the photographs of a particular calf insufficient for subsequent re-identification, the calf was excluded from survival analyses. As a measure of exposure to whale watching vessels we used two separate variables, exposure time (measured in minutes) and the total number of boat–whale interactions. The latter was used to suggest whether a higher number of boat approaches and departures could be more disturbing to animals than cumulative exposure time, possibly due to more frequent sudden ‘‘impact sounds” introduced in the water upon vessel acceleration during

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initial approach and/or departure (Beach and Weinrich, 1989; Wiley et al., 2007). ‘‘Exposure time” represents the number of minutes a whale had been exposed to whale watching vessels as a focal animal (including, in some cases, years during which females were not sexually mature). If more than one vessel was present simultaneously, the overlap in times was only included once. If a whale was not directly approached by a whale watching boat but was identified in the vicinity of the vessel (distance less than one nautical mile, visually estimated), exposure was counted as 1-min (since whales can acoustically detect the presence of the vessel at this or greater distances (Baker and Herman, 1989; Richardson et al., 1995)). ‘‘Number of interactions” represents the total number of times that a humpback whale was engaged by a whale watching vessel (one approach and one departure). Interactions are defined as when ‘‘operations of the vessel are specifically directed towards approaching and/or maintaining sight of the animal.” If more than one boat approached a whale at the same time, each boat accounted for one separate interaction. 2.3. Whale reproductive measures To examine whether there was an effect of whale watching on humpback whale reproductive fitness, we analyzed female reproductive rates and calf survival to ages one and two in order to test the ability of females both to give birth and subsequently to rear a calf. For the latter we also decided to consider survival to age 2 in order to test for both an effect on the mother’s fitness which may take several years to be expressed as well as the ability of that calf to survive on its own (calves typically wean from their mothers at approximately 1 year; Baraff and Weinrich, 1993; Baker et al., 1987). ‘‘Reproductive fitness” of individual females was analyzed by both Spearman-rank and breakpoint correlation tests (to look for additional complexity in a large data set) by comparing a female’s calving rate (determined by dividing the total number of calves each mother had between 1980 and 2006, divided by the number of reproductive years during which the mother was sighted (typically 200–400 humpback whales are seen annually, Clapham et al., 1993; unpublished data)) and measures of whale watch exposure. Because all observations of mother–calf pairs took place in the feeding grounds, our data represents calves that completed their first northward migration, probably underestimating the true number of calves born (in the North Pacific, this mortality is estimated at 15% of births – Gabriele et al., 2001). Further, ‘‘ages” herein refer to the birthday of the previous winter; hence a whale born in February 1980 is considered to be a 1-year old throughout its time on the feeding grounds in 1981. Only females that were seen with at least one calf, or those of at least 8 years old, were included in this analysis. Although 5 years has been published as the age of maturity for Gulf of Maine females (Clapham and Mayo, 1987, 1990; Clapham, 1992), more recent analysis have shown that the mean age at which females in the Gulf of Maine sub-population have their first calf is higher (7.14 ± 2.00, Weinrich, unpublished data; 7.08 overall, with a mean of 8.78 for those calves born after 1987, Robbins, 2007). To determine whether the exposure of a female to whale watching vessels affected her ability to reproduce, we examined her exposure to whale watching in each of the 2 years prior to a sighting (e.g. the year prior to a putative conception and the year during a putative pregnancy) against whether or not she had a calf in that year. Female reproductive output was also analyzed with a logistic regression in order to investigate the interplay of whale watching exposure with other variables on calf production. For every year in which a sexually mature female was seen, the dependent binary variable (presence/absence of a calf) was analyzed against expo-

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sure to whale watching the previous year and the mean number of sand lance (Ammodytes dubius) in all National Marine Fisheries Service (NMFS) ground-fish tows with non-zero values during the putative pregnancy year (obtained from the NMFS Northeast Fishery Science Center, Woods Hole, MA). Although these data represent the best quantitative time series for sand lance, a number of biases make them less than ideal for a small-scale spatial comparisons (i.e. within a subsection of the Gulf of Maine; Robbins, 2007). Correlation tests between the different whale watch exposure variables (exposure during the year prior to putative conception, the year of putative pregnancy, and cumulative lifetime exposure) showed significant relationships between them, as did several prey variables (mean annual number of sand lance caught per tow, the mean weight of sand lance caught per tow, and similar values for herring catches in the same data series). We therefore used results from the univariate tests to determine which representative variable to include in the logistic regressions. We excluded the year during which a mother had her first known calf, if these data had been used to discriminate sexual maturity. We excluded sightings of adult females for years following known calving events, because having a calf in consecutive years is a relatively rare event (Baker et al., 1987; Clapham and Mayo, 1987; Weinrich et al., 1993). We did not exclude sightings of females who had not been seen in the previous year, even though there was a chance she may have had a calf in that year. Females with calves preferentially use the south-western Gulf of Maine, and the mean calving rate of the population suggests that they do not have calves in over 50% of annual sightings. Taken together, this suggests we are not unduly biasing our data set through the inclusion of this sub-set of females. We also examined whether the exposure of a mother–calf pair to whale watching vessels affected the survival of the calf to age 1 (immediately post-weaning) and to age 2 (after one full year of independence). We examined the exposure of the mother in the year prior to birth (i.e. during pregnancy), the year that she was together with her calf, and (if applicable) to the offspring in its first year alone. Survival was indicated by a re-sighting of the offspring at any point subsequent to the age in question, whether or not it was sighted at that specific age (so an animal not re-sighted after weaning until age 7, for instance, would be scored as having survived to both ages). In order to reduce the bias for a lower probability of re-sighting animals born in the latter years of the study (i.e., less effort after the calf year), calves born after 2003 were excluded from the survival analysis. During observations in the Great South Channel, we recorded nine mother–calf pairs that were not seen in the whale watch area and there were sufficient photographs to re-identify the calves. Although this sample is limited, these pairs represent an out-group for comparison to mother–calf pairs exposed to whale watching traffic for calf survival to ages one and two, using a v2-square test. An additional 15 pairs that were seen in the same year in both habitats were excluded from this analysis. In order to control for a potential bias for young animals that, although possibly mature, could have lower reproductive output (Sugiyama, 2005; Robbins et al., 2006; Hadley et al., 2007) a subsample of 24 ‘‘prime” females (seen at least once in 1980–1984 with a calf, and then seen for at least 5 years starting in 1985) was also analyzed separately using the same methodology. At least 13 of these individuals were also still alive and calving at the end of the study. All tests described above were applied to this sub-set of reproductive females. 2.4. Statistical analyses Logistic regressions were also used to analyze calf survival. The binary dependent variables in this case were survival to age 1 (or

not) and survival to age 2 (or not), as indicated by sighting the whale in those or any subsequent year. Independent variables included whale watching exposure of mothers during pregnancy, (in the case of survival to age 2) exposure during its first year alone, the number of whale watch trips in the calf’s birth year, and the mean number of sand lance per NMFS tows as above for the calf’s birth year. For all logistic regression comparisons, we used a Bonnferroni correction factor for significance levels of alpha = 0.017 (.05/3 logistic regressions). Throughout this manuscript, mean and standard deviations were used as descriptive statistics except where noted otherwise. Data were stored in Foxpro, Access, and Excel files and analyzed with SPSS 15.0 (SPSS Inc, Chicago, IL). Breakpoint correlation tests, which were analyzed using the program SegReg.2 All data sets were tested for normality using Kolmogorov–Smirnov statistics; in many cases a bias towards lower whale watch exposure values resulted in the use of non-parametric comparisons. 3. Results 3.1. Long-term effects Of the 346 female humpback whales included in the Whale Center of New England catalogue, 283 were considered to be sexually mature, and were included in the analysis. Mean cumulative exposure time was 1746.8 min (range 1–13,746 min), and the mean number of interactions was 89.8 (range 1–614). For all female humpback whales combined the mean calving rate was 0.35 ± 0.24 calves/year. There was no correlation between an individual’s mean calving rate and either the cumulative time of whale watching exposure (Spearman-rank correlation, r = 0.008, p = 0.89; Fig. 2) or the cumulative number of boat interactions (Spearman-rank correlation, r = 0.052, p = 0.38; Fig. 3). A breakpoint regression comparing cumulative exposure time against calving rates showed a breakpoint at 1649 min, with a slight negative trend prior to that (r = 0.0001, Y(X0) = 0.163) and a stronger positive trend after the breakpoint ((r = 0.001, Y(X0) = 0.181; Fig. 4). Results from a breakpoint analysis with the number of boat interactions showed nearly identical results, with a breakpoint at 19.86 interactions. The two measures of exposure were highly correlated with each other (Spearman-rank correlation, r = 0.826, p < 0.001); as a result, further comparisons were made only to exposure time. 3.2. Influence of whale watch exposure on individual calving events Data on exposure for females in years prior to a putative pregnancy are shown in Table 2. We found that females with calves had significantly more exposure to whale watching in both the year prior to and during a possible pregnancy. Exposure during each of the 2 years were positively correlated (Spearman-rank correlation, r = 0.400, p < 0.001). Data on exposure of mother–calf pairs and the subsequent fate of the calf are presented in Tables 3 and 4. We found that there was no significant difference between those calves that were known to survive to age 1 and those not known to do so based on the mother’s whale watch exposure during pregnancy, but exposure was significantly higher in the calf year for those that returned after weaning. We also found that there was no significant difference between those calves that were known to survive to age 2 and those not known to do so based on the mother’s whale watch exposure during pregnancy or the calf year, but exposure was significantly higher in the first year alone for those calves that survived to age 2. When we compared survival to age 2 for just 2

Available from http://www.waterlog.info/segreg.htm.

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number of calves/year

1.000

0.800

0.600

0.400

0.200

0.000

R Sq Linear = 5.17E-5

0

2.500

5.000

7.500

10.000

12.500

total exposure (min) Fig. 2. The total exposure time to whale watching vessels (in minutes) and the number of calves per reproductive year for female humpback whales in the Gulf of Maine.

1.000

number of calves/year

0.800

0.600

0.400

0.200

R Sq Linear = 0.001

0.000 0

200

400

total number of interactions with boats

600

Fig. 3. The total number of whale watching vessel approaches and number of calves per reproductive year for female humpback whales in the Gulf of Maine.

Fig. 4. Breakpoint regression analysis between the total exposure time to whale watching vessels (in minutes) and the number of calves per reproductive year for female humpback whales in the Gulf of Maine.

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Table 2 Whale watch exposure (in minutes) for adult females with or without a calf. Exposure is considered for both 2 years prior and the year prior to the sighting. Results of Mann–Whitney U comparisons are included, with significant p values in bold. Calf present w adult $?

N

Mean rank exposure 2 year prior (min)

Mean rank exposure year prior (min)

Yes No p (2-tailed)

636 1751

1361.9 1132.9 0.000

1438.3 1105.2 0.000

Table 3 Whale watch exposure (in minutes) for mothers with calves known or those not known to survive to age 1. Exposure is considered for both the mother’s year of pregnancy and the year of association with her calf. Results of Mann–Whitney U comparisons are included, with significant p values in bold. Calf survival to 1?

N

Mean rank exposure during pregnancy (min)

Mean rank exposure during calf year (min)

Yes No p (2-tailed)

336 216

281.9 264.0 0.180

291.8 249.5 0.002

Table 4 Whale watch exposure (in minutes) for mothers with calves known or those not known to survive to age 2. Exposure is considered for the mother’s year of pregnancy, the year of association between the mother and her calf, and the exposure in the calf’s first year alone. Results of Mann–Whitney U comparisons are included, with significant p values in bold. Calf survival to 2?

N

Mean rank Mean rank Mean rank exposure during exposure during exposure during pregnancy (min) calf year (min) first year alone (min)

Yes 280 286.8 No 270 263.7 p (2-tailed) 0.293

281.7 268.0 0.082

315.6 234.6 0.000

each added hour (60 min) of exposure. Our index of sand lance abundance in the same year was not a significant predictor of pregnancy (p = 0.497). Only the amount of exposure of mothers during pregnancy (p = 0.025) and the prey indicator variable (p = 0.002) were significant predictors in the logistic regression for calf survival to age 1; for each extra mean increase of 10 sand lance caught in the trawls, probability of survival increased by 1.07 (SE ± 0.02). In the logistic regressions for calf return to age 2, the number of minutes of exposure during the first year alone (p < 0.001) was a significant predictor of survival (for each extra hour of whale watch exposure, odds of survival increased by 1.196 (SE ± 0.06)), as was the prey indicator variable (p = 0.02); for each extra mean increase of 10 sand lance caught in the trawls, probability of survival increased by 1.05 (SE ± 0.02). 3.3. Out-group analysis Of the nine mother–calf pairs seen only in the Great South Channel, five calves (55.5%) survived to age 1, as compared to 322 (61.1%) of the 527 pairs seen only in the whale watch area. There were also only minor differences in results between the sample of 24 ‘‘prime” reproductive females and the larger database. In the years prior to pregnancy, there was significantly more exposure in years when pregnant than in years when they were not (Mann–Whitney U-test, Z = 3.17, p = 0.002); calf survival to age 1 was associated with significantly higher exposure during the calf year (Mann–Whitney U-test, Z = 2.36, p = 0.018); and calf survival to age 2 was associated with greater exposure during the first year alone (Mann–Whitney U-test, Z = 3.85, p < 0.001). However, in the logistic regression comparisons, variables which were significant predictors of either pregnancy or calf survival in the larger sample were not significant for this group (Table 6).

4. Discussion those calves who had survived to age 1, there was no significant difference in exposure during the first year alone between those known to survive to age 2 (mean rank exposure = 168.5 min, n = 279) than those who did not return after the first year (mean rank exposure = 179.4, n = 279; Mann–Whitney U = 7963.0, Z = 0.863, p = 0.388). Results for logistic regressions are given in Table 5. Whale watch exposure in the year prior to the sighting was a significant predictor of whether or not a female was pregnant (p = 0.002), with results suggesting that odds of pregnancy increased by 1.06 for

We were not able to find negative effects of whale watching exposure on either the long-term calving rate of female humpback whales, the likelihood that a female will have a calf in a given year, or the likelihood that the calf will survive until at least 2 years of age, either by measuring the total minutes of exposure or the total number of interactions with the boats. We did, however, find a strong agreement between the two variables themselves, suggesting that either measure could suffice as an indicator of the potential for disruption in future studies.

Table 5 Results of logistic regressions for predictions of whether a female had a calf, whether a calf survived to age 1, and whether it survived to age 2 for the full data set. Degrees of freedom for all comparisons was 1. Details on the variables used in the model may be found in Section 2. Variable $ Sighted w calf or not (n = 520) (% categorized correctly = 59.8)

Calf survival to 1 (n = 365) (% categorized correctly = 63.8)

Calf survival to 2 (n = 365) (% categorized correctly = 66.3)

B

SE(B)

Wald v2

p

Exp (B)

Exposure year-1 Sand lance year-1 Constant

0.001 0.001 0.638

0.000 0.001 0.132

9.204 0.461 23.305

0.002 0.497 0.000

1.001 1.001 0.528

Exposure pregnancy WW trips –pregnancy Mean sand lance – pregnancy Constant

0.000 0.001 0.007 0.843

0.000 0.001 0.002 0.444

1.667 5.017 9.564 3.606

0.197 0.025 0.002 0.058

1.000 1.001 1.007 0.430

Exposure pregnancy WW trips – pregnancy Mean sand lance – pregnancy Exposure – first year alone Constant

0.001 0.001 0.005 0.003 1.041

0.000 0.001 0.002 0.001 0.455

3.269 1.277 5.407 13.968 5.233

0.071 0.259 0.020 0.000 0.022

1.001 1.001 1.005 1.003 0.353

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Table 6 Results of logistic regressions for predictions of whether a female had a calf, whether a calf survived to age 1, and whether it survived to age 2 for the sub-set of 24 ‘‘prime” females. Degrees of freedom for all comparisons was 1. Details on the selection of whales for this comparison and the variables used in the model may be found in Section 2. Variable $ Sighted w calf or not (n = 215) (% categorized correctly = 58.1)

Calf survival to 1 (n = 90) (% categorized correctly = 74.4)

Calf survival to 2 (n = 90) (% categorized correctly = 63.3)

B

SE(B)

Wald v2

p

Exp (B)

Exposure year-1 Sand lance year-1 Constant

0.001 0.001 0.308

0.00 0.001 0.187

3.905 0.253 2.699

0.048 0.615 0.100

1.001 1.001 0.528

Exposure pregnancy WW trips – pregnancy Mean sand lance – pregnancy Constant

0.000 0.001 0.009 0.282

0.000 0.002 0.004 0.966

0.149 0.888 3.839 0.085

0.700 0.346 0.050 0.770

1.000 1.001 1.009 0.754

Exposure pregnancy WW trips – pregnancy Mean sand lance – pregnancy Exposure – first year alone Constant

0.000 0.000 0.005 0.001 0.059

0.000 0.001 0.003 0.001 0.892

0.075 0.102 2.204 1.522 0.004

0.784 0.750 0.138 0.217 0.948

1.000 1.000 1.005 1.001 1.060

In several cases, tests showed that a higher level of whale watching exposure in a given year were significantly positively related to either the likelihood for a mother to come back with a calf in the subsequent year or for that calf to survive. This trend was also present in the univariate comparisons of the sub-sample that included only more mature females and their offspring, which were used to eliminate a potential bias for less productive younger mothers. Taken literally, these findings would suggest that whale watching is beneficial for calving. We suggest, however, that this effect is merely an artefact of the tendency of whales to return to areas where resources are abundant and likely to be available. Numerous authors have noted the strong known matrilineal fidelity of individuals to both generalized preferred feeding areas (Baker et al., 1990, 1993a,b; Palsbøll et al., 1995), and to even more specific regions within the feeding grounds (Weinrich, 1998; Stevick et al., 2006). This is likely a strategy to maximize the whale’s ability to find the resources (especially prey) that they need, which are at least somewhat predictable in space and time. Several studies (Robbins et al., 2001; Robbins, 2007) have shown the importance of the south-western Gulf of Maine for reproductive females and mothers with calves, and use of this habitat may supersede any potential effect of the exposure to whale watching traffic. Whale watching boats will also likely target these areas to increase the likelihood of finding whales and/or whale aggregations. Hence, whales spending the maximum time in a prime habitat are presumably the most fit, but may therefore also become the most exposed, animals. It should also be noted that because of these confounding variables, there could be a real negative effect from whale watch exposure while our analysis would still show a positive relationship. However, we would not conclude a negative impact until the effect size was great enough to create a negative slope, by which time the impact would be considerable. While it is difficult to resolve this relationship, the potential to mask possible effects should be considered. For survival to age 2, the logistic regression showed that calves had a higher chance to survive if the mother had higher whale watching exposure during pregnancy and if the calf had been exposed to higher whale watching traffic during its first independent year. This is likely a combination of the similarity of habitat preferences between a mother and her offspring (Clapham and Mayo, 1987, 1990; Weinrich, 1998), and the increased likelihood to survive to age 2 for a whale that survived its initial period of independence. In other words, if mortality happened at or near weaning, its exposure score during year one would be zero. The lack of any significant difference in the comparison of exposure periods for animals who did or did not survive to age 2 for only those

individuals known to survive to age 1 underscores the importance of this effect. In addition, the suitability of sand lance, an easily caught prey item for bottom-feeding juvenile humpback whales in the whale watch area, may have contributed greatly to survival of young animals that spent a significant portion of their first year in the whale watch area (Hain et al., 1995; Stimpert et al., 2006). While we believe that any positive relationships between whale watch exposure and reproduction are coincidental, it is more important that our results do not suggest that whale watching exposure, even as intense as it is in our study area, negatively affects a female’s reproductive rate or the return (and survival) of their calves. Instead, it seems that other factors, likely including prey availability, were more important in these determinations. This may, then, place the whales in the aforementioned class of animals that are obligated to remain in an area despite whale watch pressure. Still, given the high exposure level of the study population, the lack of any general signal of deleterious effects is notable. Further support of this finding comes from the initial evidence that post-weaning survival of calves was similar between those whales seen in the heavily exposed whale watch area and in the relatively remote Great South Channel, despite the limited sample size in the latter habitat and the limited strength of our comparison. It should be noted that there may also be a bias against recapture of Great South Channel calves, since offspring are likely to initially return to their natal site even within the feeding grounds (Weinrich, 1998), where our coverage has remained limited. Juveniles in many mammalian species, including marine mammals, are most likely to also explore alternate or novel habitats (Sargeant, 1976; Pereira and Fairbanks, 1993), however, and sightings of these former calves in the whale watch area is also possible (it was the case for all five of the re-photographed Great South Channel calves in this comparison). A more detailed analysis of reproduction in this or similar remote habitats also used by this population could be an important extension of our work. While we feel that our measures of individual whale watching exposure are an in index of whale watching pressure on study animals, certainly the cumulative time of whale watching exposure on these whales is vastly under-estimated. The whale watching industry off of southern New England is very large, with over 15 whale watching companies on Stellwagen Bank alone as of 1990 (Rumage, 1990); this number has slightly increased since then (D. Wiley, pers. comm.). Although we placed observers on several companies annually (often operating out of different ports, each with multiple boats), our data certainly represents only a fraction of the total whale watching exposure that each animal received.

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Our data appears to be representational, however; Rumage (1990) notes a rapid increase in the number of whale watch cruises from 1980 to 1985, then a levelling from 1985 to 1990; O’Connor et al. (2009) then note a slight decrease in whale watch passengers (with no comment on the number of cruises) from 1998 to 2008, but still maintaining a very high volume. Both the 1980–1990 trend and the continued high level from 1998 to 2005 are apparent in our coverage trends (Table 1). Unless the individuals in our data are a biased sub-set of those exposed to the industry at large (and there is no reason to think this is case), having the true measures of exposure would have increased the magnitude of the findings, but they would have not changed our conclusions. Since Stellwagen Bank and Jeffreys Ledge are sites where there is significant vessel traffic in addition to whale watching, using measurements of whale watch exposure alone may not be as important as they would be in understanding impacts as in other, more pristine areas such as Shark Bay, Australia (Bejder, 2005; Bejder et al., 2006) or Doubtful Sound, New Zealand (Lusseau, 2004) where whale watching represents a significant portion of the total vessel traffic to which the animals are exposed. Our whale watch area is, in fact, used by multitudes of commercial fishing vessels, recreational boaters, and large commercial vessels using numerous New England ports. Acoustic recordings made near whales have shown that boat noise is often audible during daylight hours when no whale watch boats are present (Scheifele and Darre, 2005; Hatch et al., 2008), so whales are likely exposed to vessel noise, and its associated disturbance, at times not measured by whale watch exposure. However, this is still unlikely to affect our conclusions unless there is a sizeable discrepancy between whale watch exposure and the actual relative amount of time a whale spent in the region. Since whale watch sighting data has even been used to describe whale occurrence and occupancy patterns in the area (Clapham et al., 1993), this is an unlikely bias. However, this population could be less sensitized to the presence of any boats, and are therefore less likely to be impacted by whale watching. Despite the ‘‘long-term” nature of this study, we only examined the potential impacts of whale watching on humpback whales over a fraction of their lives and we take into account only some parameters of the population fitness. Humpbacks are thought to live for 50 or more years (Chittleborough, 1959; Best, 2006), so this study at best addresses the effects for approximately half of their lives. It is possible that long-term exposure to whale watching, and to other vessel traffic, may eventually impact individuals through causing hearing damage (e.g. Erbe, 2002) or chronic stress, leading to an eventual decrease in fitness. To address this, we used our subsample of 24 whales known to be alive for a significant portion of the study period, all of whom were using the habitat prior to the point where any acclimation to whale watching might have taken place (Watkins, 1986), and found no evidence of negative effects of whale watch exposure. However, in the logistic regression comparisons using this sub-sample, the significant positive relationships between whale watch exposure and either pregnancy and/or calf survival seen in the larger sample were not repeated. Hence, there might be a somewhat lower tolerance to whale watch exposure among these whales than in those animals that developed and matured in the presence of the whale watch industry. Our results are also not entirely free from other suggestions of impacts at some times or to some individuals. In the breakpoint correlation analysis of exposure and lifetime calving rates, there was a slight negative relationship among those whales with lower lifetime exposure, which then turned into a positive relationship at approximately 1650 min and 20 boat interactions, although the initial trend was not likely to suggest biological significance. Further, we cannot exclude the possibility that other effects are still present. Our study only looked at the reproductive fitness of moth-

ers and of calf survival to age 1 and 2. Potential effects on recruitment rates, or on adult males, were not examined in this study. Finally, at times of low prey availability, stressors such as whale watching may combine with other factors to produce results not seen at other times (Lusseau et al., 2008); limitations in our prey availability data prevented such detailed comparisons herein. It should also be noted that the North Atlantic humpback whale population as a whole is growing at a slower rate than other populations world-wide, and well below their maximum growth rate. Stevick et al. (2003a,b) present a growth rate of 3.15% for the population based on breeding ground counts between 1979 and 1993. For the Gulf of Maine stock, growth was estimated at 6.5 ± 0.012 from 1980 to 1995 (Barlow and Clapham, 1997), and between 0% and 4.0% from 1980 to 2001 (Clapham et al., 2003). By comparison, maximum plausible growth rate for a humpback whale population is estimated at 10.6% (Clapham et al., 2001, 2006); current growth rate in some southern hemisphere stocks is believed to be approaching that rate (Bannister and Hedley, 2001; Noad et al., 2008). Why the growth rate is slower in the North Atlantic is unknown, but it opens the possibility that the lack of impacts found from whale watch exposure in this analysis may be confounded by other factors which are already impacting reproductive rates. We also cannot comment on the applicability of our findings to other populations of humpback whales, or other mysticete species. Whale watching should be carefully managed as something that can, and should not, be disturbing to wild animals, especially endangered species. However, our findings also suggest that management efforts may, at times, be best concentrated on issues in which progress may be more difficult but ultimately may have greater conservation benefits. This would include such world-wide problems for cetaceans as entanglements (Johnson, 2005; Johnson et al., 2005), collisions with vessels (Laist et al., 2001; Jensen and Silber, 2003), large-scale acoustic disturbance (Southall et al., 2007; Wright et al., 2007), pollution or the loss of important habitats (Turvey et al., 2007). Such management actions are often directed to industries that do not intend to target whales, often making measures to reduce potential impacts harder to implement. In any case, our results caution against directly extrapolating long-term effects from either short-term impact studies or the amount of whale watch exposure without carefully examining population trends with appropriate longitudinal data. Acknowledgements We thank the many people who helped collect this data over years, including C. Belt, M. Cappellino, A. Glass, R. Griffiths, A. Kurland, M. Martin, D. Morin, C. Pekarcik, K. Sardi, M. Schilling, and many other Whale Center of New England naturalists and staff over years. Fall 2006 Whale Center of New England interns M. Fynes, M. Munguia, J. Spross, and L. Yong undertook the timely process of compiling the exposure data. L. Bejder and D. Lusseau helped immensely in designing and discussing the study, and P. Hammond and H. Whitehead lent their expertise on appropriate ways to analyze the data set. Peter Stevick, Tracy Bowen, and two anonymous reviewers made valuable comments on an earlier draft of the manuscript. References Baker, C.S., Herman, L.M., 1989. Behavioral responses of humpback whales to vessel traffic: experimental and opportunistic observations. National Park Service Technical Report PS-NR-TRS-89-01. Baker, C.S., Perry, A., Herman, L.M., 1987. Reproductive histories of female humpback whale Megaptera novaeangliae in the North Pacific. Marine Ecology Progress Series 41, 103–114. Baker, C.S., Palumbi, S.R., Lambertsen, R.H., Weinrich, M.T., Calambokidis, J., O’Brien, S.J., 1990. Influence of seasonal migration on geographic partitioning of mitochondrial DNA haplotypes in humpback whales. Nature 344, 238–240.

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