Age and maternity
The genetic identifications presented here provided age for 12 whales, maternity for one, and supported the maternity assignments for another 10 (Table 4). Knowing the age of individuals allows for more precise age-specific: (1) survival and fecundity to be estimated in population models (Caswell et al. 1999; Pace et al. 2017), (2) growth curves to be developed (Moore et al. 2004; Fortune et al. 2012; Sharp et al. 2019; Stewart et al. 2021), and (3) mortality threats to be assessed (Knowlton et al. 2016). The maternity data are used for female fitness and survival estimates and provide the possibility for paternities to be assigned (Frasier et al. 2007). These familial genetic data are also used to investigate mating patterns and the effects of genetic characteristics on reproductive performance (Frasier et al. 2007, 2013). In a species with less than 400 individuals (Pace et al. 2017; Pettis et al. 2021), the linkage of these data to a dozen individuals has a significant impact on all of the studies above.
Variable mother–calf associations
Sightings apart
The analysis of mothers or calves seen apart from each other (Table 1) provided some important context for the four cases of calves initially thought to have died based on apparently early separations (Cases 1, 2, 3 and 13). In the spring months of April and May, before calves have begun to feed on solid food, one might expect to see mothers and calves staying close by and, if either were to be seen alone, it would more likely be the calf alone at the surface while the mother feeds at depth. The data suggest that the opposite is true; they are seen apart in as much as 16% of the sightings and mothers are more likely to be seen alone than calves during those months (Table 1). This unexpected finding is likely partially explained by a combination of the types of surveys conducted during those months and the feeding behavior of the mother. The majority of sightings in April and May are from planes which have shorter observation periods than those from boats, thus a calf could be easily missed if beneath the mother nursing. Also, most April sightings take place in Cape Cod Bay where surface feeding is common (Mayo and Marx 1990), thus making mothers more detectable. In some of the April/May sightings, the mother may be truly alone, but in others, the calf may be there but simply not detected due to the typically short duration of aerial observations. It is also possible that calves alone are not as detectable from the air because they are smaller and have less visible blows and thus those sightings are underrepresented. Given these caveats, it is difficult to assess the robustness of these association findings. While the existing data are clear that it is not uncommon to see mothers and calves apart in April and May, dedicated vessel-based, behavioral studies would strengthen our understanding of mother/calf associations during these months.
Starting in June, the occurrence of calves without their mothers increases steadily and by August and September, it is common for calves to never be seen with their mothers on a given day (22 and 32% respectively, Table 1B). This is a logical pattern as the calf gains independence and begins to feed on its own (Klumov 1962; Hamilton et al. 1995). The increase in separations may also be due in part to how the mothers are feeding. While surface feeding is common in April and May as stated above, August and September feeding bouts are generally focused at depths of 80 and 175 m (Baumgartner and Mate 2003). Thus, mothers are often at depth and less available to be seen with their calves. However, the potential bias introduced by this feeding behavior is likely offset by the longer observation periods that are typical of the predominant vessel-based surveys during these months. Because those observations often spanned several dive cycles, it is likely that the association data during these months are more reliable than those for April and May.
The pattern of increasing independence through the summer appears to reverses in October. While the sample size is smaller, the percentage of sightings apart drops to 17% (calves) to 21% (mothers), a substantial change from the high of 41–38% the month before (Table 1A). The majority of October sightings were in the Bay of Fundy or on Jefferys Ledge (Fig. 1). Right whale mother–calf pairs typically leave these areas in October and may come together in preparation to travel in the same way that southern right whale (E. australis) and humpback whale (Megaptera novaeangliae) mothers and calves do before departing from the calving grounds (Taber and Thomas 1982, 1984; Zoidis et al. 2014). It should be noted that all but three of the October sightings presented here occurred prior to 2011, before right whales shifted away from the Bay of Fundy and Jefferys Ledge (Hayes et al. 2018; Record et al. 2019). Due to the recent lack of October mother/calf data, it remains unknown whether this association pattern has persisted.
Do sightings apart indicate a lasting mother/calf separation?
We used to infer that any mother that was seen with a calf on the calving ground but always alone later on the feeding ground, had lost her calf. All the mothers in Cases #1, 2, 3, and 13 had such sighting patterns, yet in all four cases, the calf was in fact alive. After reviewing the data in Table 1, the single May separation captured in Case #1 (Table 4) appears to be more common than previously thought; 16% of all sightings of mothers in May are without their calves (Table 1A). Further, all but one mother seen alone more than once in April and May was also seen with her calf at some point during those months (Table 2), indicating that many early spring separations are likely temporary. Therefore, the data in Case #1 do not support the hypothesis of a lasting mother/calf separation; it is quite possible that the calf was nearby and simply not detected.
In contrast to Case #1, Case #2 appears to represent a mother and calf that separated as early as June; the calf seen alone every time during the seven subsequent sightings in every month from June through September. The mother could have been nearby for any of those sightings, but it is unusual to have no detections of the mother with, or near, the calf (Table 2 and Hamilton et al. 1995). This calf was first seen in early December and, based on its physical appearance at the time (head shape and lack of cyamids or callosity), seemed to be just a week or two old (Patrician et al. 2008). Given how well developed that calf was in September [head, shape, apparent size, and cyamid coverage (Fig. 2)], it appears this case is a combination of a relatively early birth, potentially large birth size, and rapid growth. He was the only calf for the mother, #3320, who was a minimum of 12 years old at the time (her year of birth is unknown).
Similar to Case #2, Case #3 appears to represent a lasting separation rather than a short-term one as the mother was seen alone three times over 9 days and the calf was seen alone twice over 4 days (Table 4). Furthermore, those sightings alone were in different areas that are over 200 nm (380 km) apart; the mother was on Jeffreys Ledge and the calf in the Bay of Fundy (Fig. 1).
Finally, it is unclear whether Case #13 represents a lasting separation. While Table 1 indicates that a mother seen alone in May is not uncommon, Table 2 indicates that it is rare to see a mother alone twice and never again with the calf (just three out of 17 examples). Unfortunately, the photographs from her two sightings alone in May spanned just 1 or 2 min each, so it is difficult to determine whether she was truly alone or not.
Does the separation mean a calf has been fully weaned?
While the repeated sightings apart described above indicate increased independence, they do not necessarily prove the calf was fully weaned. Observations of cetaceans are both relatively infrequent and short in duration and therefore do not provide a comprehensive picture of their behavior. For this reason, it is challenging to distinguish between a calf that is spending increased time apart from its mother but still nursing periodically and a calf that is fully weaned. Hamilton et al. (1995) only considered a calf weaned if there were 3 days with the calf alone and no sightings in between or after with the mother. Both Cases #2 and #3 meet these criteria. In Case #2, #3970 may have been weaned as early as June 17. In the June 17 sighting, he was with 13 years old #2640 in the Great South Channel and appeared to be about half the size of the older whale. The sighting spanned just 3 min. His July 5 sighting was off the New Jersey coast close to shore and the sighting lasted 2 min. There is no way to know if his mother was nearby in either of those sightings, but #3970’s large relative size in the June sighting and proximity to the shore in July, in water too shallow for his mother to be feeding below him, suggest that he may in fact have been fully weaned by June 17. Given he was likely 1–2 weeks old on December 4 (as described in the “Genetic matches” of the “Results”), he would have been approximately seven and a half months old in mid-June. While this is not much younger than the previously youngest documented weaning of a right whale at approximately 8 months (Hamilton et al. 1995), the data suggest that weaning at such a young age is rare. Further, the single early weaning example in Hamilton et al. (1995) was the result of the mother’s death, while the early weaning cases presented here and immediately below are likely the result of active, behavioral decisions by the mother (Trivers 1974; Taber and Thomas 1982).
Case #3 (#3790) also meets the Hamilton et al. (1995) criteria for weaning with #3790 weaned by August 30. Although we don’t know when #3790 was born (her first sighting was in April, see Table 4), if we use the birth date of January 5 estimated by Fortune et al. (2012), #3790 would have been 8 months when weaned.
Case #13 (#4040) does not fit the criteria for weaning but is worth noting because of the early separation (Table 4) and the rarity of the separation data for that time of year (Table 2). Case #13 was the only instance of a mother never seen with her calf in April or May even though her calf was still alive. If the two May sightings of #1308 alone represent a complete separation, given #4040 was born between December 20 and January 24, she would have been approximately 5 months old when her mother was first seen alone. Although the possibility that she was weaned by then is bolstered by the data in Table 2 and thus cannot be ruled out, given that the case does not meet the three-sightings-alone criteria, and that it would be a very young weaning, it is more likely that the calf was nearby in one or both sightings and simply not detected.
Calves associated with other mothers
The analysis discovered two cases of calves associating with mothers other than their own. Besides Frasier et al.’s (2010) report of two mothers swapping calves on the calving ground and raising each other’s calves throughout the year, Case #4 is the first time to our knowledge that a mother–calf association observed in May was not a true mother–calf pair. However, the data supporting this association are weak. Calf #3580 and #1315 were together for a short period at the beginning of the 18 min long sighting, then the calf was alone playing at the surface for the remainder of the time before, according to the field notes, he “joined mom and raced away”. There are no photographs of the association at the end of the sighting to confirm it was #1315 he rejoined, so it is possible that he in fact joined his mother #1970. She was photographed nearby less than 2 h earlier so was known to be in the area. Thus, the association with #1315 may have been short-lived.
Case #5 is a particularly interesting case where it was initially thought to be one calf with a mother when in fact that mother associated with two different calves during the observation period. When calves are nursing, they often come up for quick breaths making it difficult to get detailed photographs of their callosity. In this case, #1608 and her calf #3308 were photographed together over a 20-min period. The pair dove and when they resurfaced 10 min later, the research team approached and biopsied the calf assuming, based on the association, that it was the same calf #1608 had been with before. Both the genetics, and subsequent inspection of the photographs, showed this to be incorrect; the darted calf was #3310- the calf of #2301. Whale #3310 had joined #1608 during the dive; it is unclear whether #3308 was also still there and undetected or had swum away. Similar to Case #4 above, #3310’s association with #1608 was likely short-lived as she was seen 80 min later with her own mother, #2301. This case underscores the importance of always taking confirming photographs when biopsying even if the whales were well-photographed just minutes before the sampling event.
Physical development
Two dead whales in this study were incorrectly classified as calves of the year (Table 4). Like all mammals, the length of a right whale at a given point in time is influenced by the fitness of its mother, timing of the calf’s birth, their length at birth, and their growth rate after birth (Moore et al. 2004; Christiansen et al. 2018; Sharp et al. 2019; Stewart et al. 2021). For most right whales, many of these factors are unknown, or only partially known. Given the resulting uncertainties around length, the initial misclassification of the dead whales in Cases #6 and #7 as calves of the year based on their size is understandable. Using measurements from dead, known-age whales, Sharp et al. (2019) classified animals under 9.0 m in length as calves of the year and carcasses between 10.0 and 12.0 m as juveniles. Both of these dead whales had length measurements that fell between the calf and juvenile categories. In Case #6, #3595’s growth was only slightly smaller than average for a 1.5 years old (9.58 m), whereas in Case #7, #4505’s estimated length of 9.0 m was very small for a 3.6 + years old. Some of the shortfall in length in the latter case was likely caused by the need to estimate the length without flukes present. Still, even allowing for error, it seems #4505 was truly small for his age. With limited data, Sharp et al. (2019) found some evidence that whales in the 2010 decade were smaller than whales from previous decades. Those preliminary findings have since been borne out by Stewart et al. (2021), who found decreasing body lengths in right whales over a three-decade period. The authors discovered that a whale born in 2019 is expected to reach a maximum length one meter less than a whale born in 1981. Stunted growth was linked to entanglements in fishing gear, either the whale had been severely entangled previously or its mother had been entangled while nursing. Neither #3593 nor #4505 had evidence of a previous entanglement that would have affected their growth (#4505 died of an entanglement, but had been gear-free just a few months prior to his death) and neither of their mothers were entangled while nursing. Stewart et al. (2021) noted that stunted growth could be the result of cumulative impacts including the additional factors of shifting prey seascapes, vessel strikes, and foraging interference from vessel traffic. Climate change has definitely impacted the prey seascape for right whales since 2012 (Record et al. 2019) and those changes may have, in part, resulted in #3593 and #4505’s stunted growth.
While Cases #6 and #7 represent animals that were smaller than expected, Case #2 is clearly a case of an unusually well-developed calf (Fig. 2). By the age of 10 months, his physical features were more consistent with a 22 month old yearling. Calves can generally be distinguished from 1 or 2-year-old whales based on their size, the shape of their heads (Patrician et al. 2008), and the quantity and color of cyamids on their head. Whereas calves tend to have patches of orange cyamids (Cyamus erraticus), the callosities of whales 1 year old and older have few of this species and instead are colonized by a species that is white (Cyamus ovalis) (Rowntree 1996). Potential reasons for #3970’s advanced development are that his mother #3320 was in good condition and that condition resulted in higher quality milk, his genetics favor robust growth, he was larger than most at birth, he experienced better than average feeding conditions once he began to feed on plankton, or a combination of these factors. Given he was large by June, it seems the first two explanations are more likely as #3970 would have just begun to feed in April.
Genotyped and not cataloged
Since 2011, a relatively large percentage of whales that were biopsied as calves have not been cataloged or biopsied again (Table 3—2011–2017). This increase in unidentified calves compared to previous years is likely caused by fewer calves being well-photographed on the feeding grounds (i.e. they could not be photographically identified) and a delay in genetic re-sampling. The dates between samples in the “Genetics evidence” column in Table 4 show that, on average, it takes almost 5 years for a calf from previous years to be genetically re-sampled. The recent distribution shift, and the fact that most of the surveys in the newly occupied habitats are aerial, has exacerbated this already long delay between re-sampling events because locating and biopsying the unknown juveniles has become more challenging.
As for the biopsied calves from the earlier years (i.e. 1988–2010) that have still not been genetically re-sampled, most represent situations where either (1) the mother was seen 2 years later with a calf indicating that her previous calf likely died (Burnell 2001; Browning et al. 2010) or (2) the mother was an offshore whale and her calf may not have yet returned to inshore waters. In the latter case, the calves were only seen when they were very young before their callosities developed. These whales may still be alive but seen so rarely, if at all, that they have not been biopsied again. The possibility that some of these calves may spend their lives in other habitats is intriguing. We know that other habitats must exist at every time of year and that some whales preferentially use these unknown areas (i.e., mothers that are only seen in their calving years) (Hamilton et al. 2007). Therefore, some of these calves represent a portion of the population whose life history data are poorly tracked.
Implications for other species
While this study is focused on North Atlantic right whales, the results presented here underscore the importance of genetic sampling of young animals of other species as well. There is a tremendous variation in the behavior of wild animals, and that variability is amplified by a rapidly changing climate. Collecting samples from individuals as early as possible without causing harm increases the chances of recognizing them in the future, thus improving our ability to more accurately track the vital rates of a population. While the rationale for early sampling applies to many mammals, it is particularly important for studies of other large cetaceans. Whales tend to have large geographic ranges and only sporadic opportunities for observation due to the challenges inherent in working at sea with long-diving animals. This means that cetologists have to piece together individual whales’ life stories using only partial data from relatively few observations. For this reason, sampling calves on their birthing grounds while they are still associated with their mothers increases the chance that data on age, maternity, and survival, among others, will be as complete as possible.